ORCID Profile
0000-0001-6831-3677
Current Organisation
University of Sydney
Does something not look right? The information on this page has been harvested from data sources that may not be up to date. We continue to work with information providers to improve coverage and quality. To report an issue, use the Feedback Form.
Research Topics
In Research Link Australia (RLA), "Research Topics" refer to ANZSRC FOR and SEO codes. These topics are either sourced from ANZSRC FOR and SEO codes listed in researchers' related grants or generated by a large language model (LLM) based on their publications.
Top 5 Research Topics
ANZSRC Field of Research (FoR)
Genetics | Sociobiology And Behavioural Ecology | Population, Ecological and Evolutionary Genetics | Evolutionary Biology | Ethology and Sociobiology | Gene Expression | Epigenetics (incl. Genome Methylation and Epigenomics) | Invasive Species Ecology | Behavioural Ecology | Other Artificial Intelligence | Applied Mathematics | Genetics Not Elsewhere Classified | Animal Production | Biological Mathematics | Zoology | Animal Breeding | Evolutionary Impacts of Climate Change | Life Histories | Genomics | Plant Physiology | Genome Structure | Genetic Development (Incl. Sex Determination) | Invertebrate Biology | Molecular Evolution | Meiosis And Recombination | Animal Systematics and Taxonomy | Biogeography and Phylogeography | Biological Adaptation
ANZSRC Socio-Economic Objective (SEO)
Biological sciences | Expanding Knowledge in the Biological Sciences | Control of Animal Pests, Diseases and Exotic Species in Farmland, Arable Cropland and Permanent Cropland Environments | Livestock not elsewhere classified | Animal Production and Animal Primary Products not elsewhere classified | Minor livestock (e.g. horses, goats, deer) | Control of Pests, Diseases and Exotic Species at Regional or Larger Scales | Control of Animal Pests, Diseases and Exotic Species in Forest and Woodlands Environments | Border Biosecurity (incl. Quarantine and Inspection) | Climate Change Adaptation Measures | Political science and public policy | Mathematical sciences | Pre-Border Biosecurity | Flora, Fauna and Biodiversity of environments not elsewhere classified | Control of pests and exotic species | Health not elsewhere classified |
Related Links
Publications
Only full-sibling families evolved eusociality
Publisher: Springer Science and Business Media LLC
Date: 23-03-2011
DOI: 10.1038/NATURE09832
Abstract: Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010) Nowak et al. reply. The paper by Nowak et al. has the evolution of eusociality as its title, but it is mostly about something else. It argues against inclusive fitness theory and offers an alternative modelling approach that is claimed to be more fundamental and general, but which, we believe, has no practical biological meaning for the evolution of eusociality. Nowak et al. overlook the robust empirical observation that eusociality has only arisen in clades where mothers are associated with their full-sibling offspring that is, in families where the average relatedness of offspring to siblings is as high as to their own offspring, independent of population structure or ploidy. We believe that this omission makes the paper largely irrelevant for understanding the evolution of eusociality.
Social Insects: Behavioral Genetics
Publisher: Elsevier
Date: 2009
Worker reproduction in mixed-species colonies of honey bees
Publisher: Oxford University Press (OUP)
Date: 2009
Policing of adult honey bees with activated ovaries is error prone
Publisher: No publisher found
Date: 2002
A thelytokous lineage of socially parasitic honey bees has retained heterozygosity despite at least 10 years of inbreeding
Publisher: Wiley
Date: 05-11-2011
DOI: 10.1111/J.1558-5646.2010.01164.X
Abstract: The honey bee population of South Africa is ided into two subspecies: a northern population in which queenless workers reproduce arrhenotokously and a southern one in which workers reproduce thelytokously. A hybrid zone separates the two, but on at least three occasions the northern population has become infested by reproductive workers derived from the southern population. These parasitic workers lay in host colonies parthenogenetically, resulting in yet more parasites. The current infestation is 20-year old--surprising because an asexual lineage is expected to show a decline in vigor over time due to increasing homozygosity. The decline is expected to be acute in honey bees, where homozygosity at the sex locus is lethal. We surveyed colonies from the zone of infestation and genotyped putative parasites at two sets of linked microsatellite loci. We confirm that there is a single clonal lineage of parasites that shows minor variations arising from recombination events. The lineage shows high levels of heterozygosity, which may be maintained by selection against homozygotes, or by a reduction in recombination frequency within the lineage. We suggest that the clonal lineage can endure the costs of asexual reproduction because of the fitness benefits of its parasitic life history.
Estimating the density of honey bee (Apis mellifera) colonies using trapped drones: area sampled and drone mating flight distance
Publisher: Springer Science and Business Media LLC
Date: 15-08-2019
Emergency queens in Tetragonula carbonaria (Smith, 1854) (Hymenoptera: Apidae: Meliponini)
Publisher: Wiley
Date: 24-06-2015
DOI: 10.1111/AEN.12104
Genetic diversity promotes homeostasis in insect colonies
Publisher: Elsevier BV
Date: 08-2007
DOI: 10.1016/J.TREE.2007.06.001
Abstract: Although most insect colonies are headed by a singly mated queen, some ant, wasp and bee taxa have evolved high levels of multiple mating or 'polyandry'. We argue here that a contributing factor towards the evolution of polyandry is that the resulting genetic ersity within colonies provides them with a system of genetically based task specialization, enabling them to respond resiliently to environmental perturbation. An alternate view is that genetic contributions to task specialization are a side effect of multiple mating, which evolved through other causes, and that genetically based task specialization now makes little or no contribution to colony fitness.
Kin conflict in insect societies: A new epigenetic perspective
Publisher: Elsevier BV
Date: 07-2012
DOI: 10.1016/J.TREE.2012.02.005
Abstract: The social hymenopterans (ants, wasps and bees) have all the enzymatic and genetic mechanisms necessary for the functional modification of DNA by methylation. Methylation appears to play a central role in shaping the developmental processes that give rise to the different castes. However, could DNA methylation have other roles in social insects? Theoretical arguments predict that male and female hymenopterans can be in conflict over the reproductive potential of their female offspring. An exciting prospect for future research is to examine the possibility that queens and males imprint the genomes of their gametes using DNA methylation to manipulate the reproductive potential of their progeny in ways that favour the inclusive fitness of the parent.
What's killing American honey bees?
Publisher: Public Library of Science (PLoS)
Date: 12-06-2007
Increase in dance imprecision with decreasing foraging distance in the honey bee Apis mellifera L. is partly explained by physical constraints
Publisher: Springer Science and Business Media LLC
Date: 28-07-2005
DOI: 10.1007/S00359-005-0034-0
Abstract: Honey bee foragers communicate the direction and distance of both food sources and new nest sites to nest mates by means of a symbolic dance language. Interestingly, the precision by which dancers transfer directional information is negatively correlated with the distance to the advertised food source. The 'tuned-error' hypothesis suggests that colonies benefit from this imprecision as it spreads recruits out over a patch of constant size irrespective of the distance to the advertised site. An alternative to the tuned-error hypothesis is that dancers are physically incapable of dancing with great precision for nearby sources. Here we revisit the tuned-error hypothesis by studying the change in dance precision with increasing foraging distance over relatively short distances while controlling for environmental influences. We show that bees indeed increase their dance precision with the increase in foraging distance. However, we also show that dance performed by swarm-scouts for a nearby (30 m) nest site, where there could be no benefit to imprecision, are either without or with only limited directional information. This result suggests that imprecision in dance communication is caused primarily by physical constraints in the ability of dancers to turn around quickly enough when the advertised site is nearby.
The frequency of arrhenotoky in the normally thelytokous Apis mellifera capensis worker and the Clone reproductive parasite
Publisher: Springer Science and Business Media LLC
Date: 30-04-2015
Genetic evaluation of a novel system for controlled mating of the honeybee, apis mellifera
Publisher: Oxford University Press (OUP)
Date: 27-11-2010
Abstract: Many apiculturally important traits of the honeybee have medium to high heritabilities and are therefore capable of strong response to selection. However, the natural mating system of honeybees makes it difficult to exclude unselected males from matings and necessitates expensive procedures like artificial insemination or isolated mating stations. By manipulating ambient light and temperature, an Australian queen breeder has developed a novel system that delays the flight time of selected queens and drones. To assess the efficacy of this "Horner system," drones and their assumed worker offspring were genotyped using microsatellite loci to test whether the workers were exclusively sired by the selected drones. The Horner system was found to provide at least 85% control of matings, equivalent to a 48% increase in the selection differential, when queens and drones are selected in a breeding program.
Population structuring of the ubiquitous stingless bee Tetragonisca angustula in southern Brazil as revealed by microsatellite and mitochondrial markers
Publisher: Wiley
Date: 30-08-2017
Abstract: Tetragonisca angustula is one of the most widespread stingless bees in the Neotropics. This species swarms frequently and is extremely successful in urban environments. In addition, it is one of the most popular stingless bee species for beekeeping in Latin America, so nest transportation and trading is common. Nest transportation can change the genetic structure of the host population, reducing inbreeding and increasing homogenization. Here, we evaluate the genetic structure of 17 geographic populations of T. angustula in southern Brazil to quantify the level of genetic differentiation between populations. Analyses were conducted on partially sequenced mitochondrial genes and 11 microsatellite loci of 1002 workers from 457 sites distributed on the mainland and on 3 islands. Our results show that T. angustula populations are highly differentiated as demonstrated by mitochondrial DNA (mtDNA) and microsatellite markers. Of 73 haplotypes, 67 were population-specific. MtDNA ersity was low in 9 populations but microsatellite ersity was moderate to high in all populations. Microsatellite data suggest 10 genetic clusters and low level of gene flow throughout the studied area. However, physical barriers, such as rivers and mountain ranges, or the presence or absence of forest appear to be unrelated to population clusters. Factors such as low dispersal, different ecological conditions, and isolation by distance are most likely shaping the population structure of this species. Thus far, nest transportation has not influenced the general population structure in the studied area. However, due to the genetic structure we found, we recommend that nest transportation should only occur within and between populations that are genetically similar.
Queen mating frequency and maternity of males in the stingless bee Trigona carbonaria Smith
Publisher: Springer Science and Business Media LLC
Date: 08-2002
Conserved numts mask a highly divergent mitochondrial-COI gene in a species complex of Australian stingless bees Tetragonula (Hymenoptera: Apidae)
Publisher: Informa UK Limited
Date: 17-09-2019
Genetic structure of a giant honey bee (Apis dorsata) population in northern Thailand: Implications for conservation
Publisher: Wiley
Date: 08-03-2013
The Mechanistic, Genetic, and Evolutionary Basis of Worker Sterility in the Social Hymenoptera
Publisher: Elsevier
Date: 2016
Subfamily-dependent alternative reproductive strategies in worker honeybees
Publisher: Wiley
Date: 24-11-2017
DOI: 10.1111/MEC.14417
Abstract: Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are keys to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study, we show that in honeybee (Apis mellifera) colonies, the social environment of a worker, that is, the presence and relatedness of the queens in a worker's natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker's subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicates that honeybee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter.
Anthropogenic hive movements are changing the genetic structure of a stingless bee (Tetragonula carbonaria) population along the east coast of Australia
Publisher: Springer Science and Business Media LLC
Date: 20-12-2018
DNA methylation of Kr-h1 is involved in regulating ovary activation in worker honeybees (Apis mellifera)
Publisher: Springer Science and Business Media LLC
Date: 13-10-2016
Anarchistic queen honey bees have normal queen mandibular pheromones
Publisher: Springer Science and Business Media LLC
Date: 02-2005
The distribution of thelytoky, arrhenotoky and androgenesis among castes in the eusocial Hymenoptera
Publisher: Springer Science and Business Media LLC
Date: 21-12-2018
Maintenance and loss of heterozygosity in a thelytokous lineage of honey bees (apis mellifera capensis)
Publisher: Wiley
Date: 02-02-2012
DOI: 10.1111/J.1558-5646.2011.01543.X
Abstract: An asexual lineage that reproduces by automictic thelytokous parthenogenesis has a problem: rapid loss of heterozygosity resulting in effective inbreeding. Thus, the circumstances under which rare asexual lineages thrive provide insights into the trade-offs that shape the evolution of alternative reproductive strategies across taxa. A socially parasitic lineage of the Cape honey bee, Apis mellifera capensis, provides an ex le of a thelytokous lineage that has endured for over two decades. It has been proposed that cytological adaptations slow the loss of heterozygosity in this lineage. However, we show that heterozygosity at the complementary sex determining (csd) locus is maintained via selection against homozygous diploid males that arise from recombination. Further, because zygosity is correlated across the genome, it appears that selection against diploid males reduces loss of homozygosity at other loci. Selection against homozygotes at csd results in substantial genetic load, so that if a thelytokous lineage is to endure, unusual ecological circumstances must exist in which asexuality permits such a high degree of fecundity that the genetic load can be tolerated. Without these ecological circumstances, sex will triumph over asexuality. In A. m. capensis, these conditions are provided by the parasitic interaction with its conspecific host, Apis mellifera scutellata.
Maternity of replacement queens in the thelytokous Cape honey bee Apis mellifera capensis
Publisher: Springer Science and Business Media LLC
Date: 27-10-2010
Factors affecting the dynamics of the honeybee (Apis mellifera) hybrid zone of South Africa
Publisher: Springer Science and Business Media LLC
Date: 12-09-2008
Abstract: Hybrid zones are found wherever two populations distinguishable on the basis of heritable characters overlap spatially and temporally and hybridization occurs. If hybrids have lower fitness than the parental types a tension zone may emerge, in which there is a barrier to gene flow between the two parental populations. Here we discuss a hybrid zone between two honeybee subspecies, Apis mellifera capensis and A. m. scutellata and argue that this zone is an ex le of a tension zone. This tension zone is particularly interesting because A. m. capensis can be a lethal social parasite of A. m. scutellata. However, despite its parasitic potential, A. m. capensis appears to be unable to increase its natural range unassisted. We propose three interlinked mechanisms that could maintain the South African honeybee hybrid zone: (1) low fitness of intercrossed and genetically mixed colonies arising from inadequate regulation of worker reproduction (2) higher reproductive success of A. m. scutellata via both high dispersal rates into the hybrid zone and increased competitiveness of males, countered by (3) the parasitic nature of A. m. capensis.
Genetic architecture of the Tetragonula carbonaria species complex of Australian stingless bees (Hymenoptera: Apidae: Meliponini)
Publisher: Oxford University Press (OUP)
Date: 05-06-2014
DOI: 10.1111/BIJ.12292
Measuring the cost of worker reproduction in honeybees: Work tempo in an 'anarchic' line
Publisher: Springer Science and Business Media LLC
Date: 2004
Queenless colonies of the Asian red dwarf honey bee (Apis florea) are infiltrated by workers from other queenless colonies
Publisher: Oxford University Press (OUP)
Date: 2009
Ancestral monogamy shows kin selection is key to the evolution of eusociality
Publisher: American Association for the Advancement of Science (AAAS)
Date: 30-05-2008
Abstract: Close relatedness has long been considered crucial to the evolution of eusociality. However, it has recently been suggested that close relatedness may be a consequence, rather than a cause, of eusociality. We tested this idea with a comparative analysis of female mating frequencies in 267 species of eusocial bees, wasps, and ants. We found that mating with a single male, which maximizes relatedness, is ancestral for all eight independent eusocial lineages that we investigated. Mating with multiple males is always derived. Furthermore, we found that high polyandry ( effective mates) occurs only in lineages whose workers have lost reproductive totipotency. These results provide the first evidence that monogamy was critical in the evolution of eusociality, strongly supporting the prediction of inclusive fitness theory.
Multiple paternity or multiple queens: Two routes to greater intracolonial genetic diversity in the eusocial Hymenoptera
Publisher: Wiley
Date: 14-04-2008
DOI: 10.1111/J.1420-9101.2008.01532.X
Abstract: Understanding the evolution of multiple mating by females (polyandry) is an important question in behavioural ecology. Most leading explanations for polyandry by social insect queens are based upon a postulated fitness benefit from increased intracolonial genetic ersity, which also arises when colonies are headed by multiple queens (polygyny). An indirect test of the genetic ersity hypotheses is therefore provided by the relationship between polyandry and polygyny across species, which should be negative if the genetic ersity hypotheses are correct. Here, we conduct a powerful comparative investigation of the relationship between polyandry and polygyny for 241 species of eusocial Hymenoptera (ants, bees and wasps). We find a clear and significant negative relationship between polyandry and polygyny after controlling for phylogeny. These results strongly suggest that fitness benefits resulting from increased intracolonial genetic ersity have played an important role in the evolution of polyandry, and possibly polygyny, in social insects.
Nature versus nurture in social insect caste differentiation
Publisher: Elsevier BV
Date: 05-2010
DOI: 10.1016/J.TREE.2009.12.001
Abstract: Recent evidence for genetic effects on royal and worker caste differentiation from erse social insect taxa has put an end to the view that these phenotypes stem solely from a developmental switch controlled by environmental factors. Instead, the relative influences of genotypic and environmental effects on caste vary among species, ranging from largely environmentally controlled phenotypes to almost purely genetic systems. Disentangling the selective forces that generate variation for caste predisposition will require characterizing the genetic mechanisms underlying this variation, and identifying particular life-history strategies and kin structures associated with strong genetic effects on caste.
Regulation of oogenesis in the queen honey bee (Apis mellifera)
Publisher: Cold Spring Harbor Laboratory
Date: 09-03-2021
DOI: 10.1101/2021.03.08.434480
Abstract: In the honey bee ( Apis mellifera ), queen and worker castes originate from identical genetic templates but develop into different phenotypes. Queens lay up to 2,000 eggs daily whereas workers are sterile in the queen’s presence. Periodically queens stop laying during swarming, when resources are scarce in winter and when they are confined to a cage by beekeepers. We used confocal microscopy and gene expression assays to investigate the control of oogenesis in honey bee queen ovaries. We show that queens use different combination of ‘checkpoints’ to regulate oogenesis compared to honey bee workers and other insect species. However, both queen and worker castes use the same programmed cell death pathways to terminate oocyte development at their caste-specific checkpoints. Our results also suggest that the termination of oogenesis in queens is driven by nutritional stress. Thus, queens may regulate oogenesis via the same regulatory pathways that were utilised by ancestral solitary species but have adjusted physiological checkpoints to suit their highly-derived life history. Honey bee queens regulate oogenesis using a different combination of ‘checkpoints’ to workers, but both castes use the same molecular pathways.
When workers disunite: Intraspecific parasitism by eusocial bees
Publisher: Annual Reviews
Date: 2008
DOI: 10.1146/ANNUREV.ENTO.53.103106.093515
Abstract: One of the most obvious characteristics of an insect society is reproductive cooperation. Yet insect colonies are vulnerable to reproductive parasitism, both by workers from their own colony and by workers from others. Little is known about the mechanisms insect societies have evolved to protect themselves from being exploited from within and outside the colony and the mechanisms that social parasites have evolved to circumvent these mechanisms. Here we showcase recently discovered cases of intraspecific parasitism by workers in eusocial bees. These discoveries overturn the widespread view that insect colonies are like fortresses populated by female eunuchs, and yield important insights into the mechanisms that normally enforce functional worker sterility.
Different policing rates of eggs laid by queenright and queenless anarchistic honey-bee workers (Apis mellifera L.)
Publisher: Springer Science and Business Media LLC
Date: 09-2003
Modelling honey bee queen mating as a measure of feral colony density
Publisher: Elsevier BV
Date: 12-2012
Extreme polyandry AIDS the establishment of invasive populations of a social insect
Publisher: Springer Science and Business Media LLC
Date: 23-08-2017
DOI: 10.1038/HDY.2017.49
Queenless colonies contribute to the male breeding population at honey bee drone congregation areas
Publisher: Springer Science and Business Media LLC
Date: 10-08-2019
The Genetic Architecture of Honeybee Breeding
Publisher: Elsevier
Date: 2010
Asian hive bees, Apis cerana, modulate dance communication in response to nectar toxicity and demand
Publisher: Elsevier BV
Date: 12-2012
Intergenerational reproductive parasitism in a stingless bee
Publisher: Wiley
Date: 23-09-2009
Queen pheromone regulates programmed cell death in the honey bee worker ovary
Publisher: Wiley
Date: 20-06-2016
DOI: 10.1111/IMB.12250
Abstract: In social insect colonies the presence of a queen, secreting her pheromones, is a key environmental cue for regulating the reproductive state of workers. However, until recently the proximate molecular mechanisms underlying facultative worker sterility were unidentified. Studies into worker oogenesis in the honey bee (Apis mellifera) have indicated that programmed cell death is central to the regulation of oogenesis. Here we investigate how queen pheromone, age of the worker and ovary state affect both programmed cell death and cell number in worker ovaries. We describe a novel method to simultaneously measure programmed cell death (caspase activity) and live cell number (estimated from the amount of adenosine triphosphate) in an insect tissue. Workers exposed to queen pheromone have higher levels of caspase activity in the ovary than those not exposed. Our results suggest that queen pheromone triggers programmed cell death at the mid-oogenesis checkpoint causing the abortion of worker oocytes and reproductive inhibition of the worker caste. Nonetheless, high caspase activity is present in activated ovaries from workers not exposed to queen pheromone. This caspase activity is most likely to be from the nurse cells undergoing programmed cell death, in late oogenesis, for normal oocyte development. Our study shows that the social environment of an organism can influence programmed cell death within a tissue.
The frequency of thelytokous parthenogenesis in European-derived Apis mellifera virgin queens
Publisher: Springer Science and Business Media LLC
Date: 08-05-2019
Towards a molecular definition of worker sterility: Differential gene expression and reproductive plasticity in honey bees
Publisher: Wiley
Date: 10-2006
The reproductive dilemmas of queenless red dwarf honeybee (Apis florea) workers
Publisher: Springer Science and Business Media LLC
Date: 02-08-2006
Reply to Soley: DNA methylation marks are stably transferred across generations in honey bees
Publisher: Proceedings of the National Academy of Sciences
Date: 06-07-2021
The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera.
Publisher: Springer Science and Business Media LLC
Date: 28-07-2005
DOI: 10.1007/S00359-005-0035-Z
Abstract: Honey bee workers maintain the brood nest of their colony within a narrow temperature range of 34.5+/-1.5 degrees C, implying that there are significant fitness costs if brood is reared outside the normal range. However, the effects of abnormal incubation temperatures are subtle and not well documented. Here we show that short-term learning and memory abilities of adult workers are affected by the temperature they experienced during pupal development. In contrast, long-term learning and memory is not significantly affected by rearing temperature. Furthermore, we could detect no effects of incubation temperature on fluctuating asymmetry, as a measure of developmental stability, in workers, queens or drones. We conclude that the most important consequence of abnormal rearing temperatures are subtle neural deficiencies affecting short-term memory rather than physical abnormalities.
Genetic origins of honey bees (Apis mellifera) on Kangaroo Island and Norfolk Island (Australia) and the Kingdom of Tonga
Publisher: Springer Science and Business Media LLC
Date: 07-01-2019
A scientific note on a simple method for karyotyping honey bee (Apis mellifera) eggs
Publisher: Springer Science and Business Media LLC
Date: 25-11-2010
Honey bee nest thermoregulation: Diversity promotes stability
Publisher: American Association for the Advancement of Science (AAAS)
Date: 16-07-2004
Abstract: A honey bee colony is characterized by high genetic ersity among its workers, generated by high levels of multiple mating by its queen. Few clear benefits of this genetic ersity are known. Here we show that brood nest temperatures in genetically erse colonies (i.e., those sired by several males) tend to be more stable than in genetically uniform ones (i.e., those sired by one male). One reason this increased stability arises is because genetically determined ersity in workers' temperature response thresholds modulates the hive-ventilating behavior of in idual workers, preventing excessive colony-level responses to temperature fluctuations.
Selection on overdominant genes maintains heterozygosity along multiple chromosomes in a clonal lineage of honey bee
Publisher: Wiley
Date: 02-09-2014
DOI: 10.1111/EVO.12231
Abstract: Correlations between fitness and genome-wide heterozygosity (heterozygosity-fitness correlations, HFCs) have been reported across a wide range of taxa. The genetic basis of these correlations is controversial: do they arise from genome-wide inbreeding ("general effects") or the "local effects" of overdominant loci acting in linkage disequilibrium with neutral loci? In an asexual thelytokous lineage of the Cape honey bee (Apis mellifera capensis), the effects of inbreeding have been homogenized across the population, making this an ideal system in which to detect overdominant loci, and to make inferences about the importance of overdominance on HFCs in general. Here we investigate the pattern of zygosity along two chromosomes in 42 workers from the clonal Cape honey bee population. On chromosome III (which contains the sex-locus, a gene that is homozygous-lethal) and chromosome IV we show that the pattern of zygosity is characterized by loss of heterozygosity in short regions followed by the telomeric restoration of heterozygosity. We infer that at least four selectively overdominant genes maintain heterozygosity on chromosome III and three on chromosome IV via local effects acting on neutral markers in linkage disequilibrium. We conclude that heterozygote advantage and local effects may be more common and evolutionarily significant than is generally appreciated.
DNA methylation is not a driver of gene expression reprogramming in young honey bee workers
Publisher: Wiley
Date: 08-08-2021
DOI: 10.1111/MEC.16098
Abstract: The presence of DNA methylation marks within genic intervals, also called gene body methylation, is an evolutionarily‐conserved epigenetic hallmark of animal and plant methylomes. In social insects, gene body methylation is thought to contribute to behavioural plasticity, for ex le between foragers and nurse workers, by modulating gene expression. However, recent studies have suggested that the majority of DNA methylation is sequence‐specific, and therefore cannot act as a flexible mediator between environmental cues and gene expression. To address this paradox, we examined whole‐genome methylation patterns in the brains and ovaries of young honey bee workers that had been subjected to ergent social contexts: the presence or absence of the queen. Although these social contexts are known to bring about extreme changes in behavioral and reproductive traits through differential gene expression, we found no significant differences between the methylomes of workers from queenright and queenless colonies. In contrast, thousands of regions were differentially methylated between colonies, and these differences were not associated with differential gene expression in the subset of genes examined. Methylation patterns were highly similar between brain and ovary tissues and only differed in nine regions. These results strongly indicate that DNA methylation is not a driver of differential gene expression between tissues or behavioral morphs. Finally, despite the lack of difference in methylation patterns, queen presence affected the expression of all four DNA methyltransferase genes, suggesting that these enzymes have roles beyond DNA methylation. Therefore, the functional role of DNA methylation in social insect genomes remains an open question.
Asexually produced cape honeybee queens (apis mellifera capensis) reproduce sexually
Publisher: Oxford University Press (OUP)
Date: 20-07-2011
Abstract: Unmated workers of the Cape honeybee Apis mellifera capensis can produce female offspring including daughter queens. As worker-laid queens are produced asexually, we wondered whether these asexually produced in iduals reproduce asexually or sexually. We s led 11 colonies headed by queens known to be the clonal offspring of workers and genotyped 23 worker offspring from each queen at 5 microsatellite loci. Without exception, asexually produced queens produced female worker offspring sexually. In addition, we report the replacement of a queen by her asexually produced granddaughter, with this asexually produced queen also producing offspring sexually. Hence, once a female larva is raised as a queen, mating and sexual reproduction appears to be obligatory in this subspecies, despite the fact that worker-laid queens are derived from asexual lineages.
Paternity frequency and maternity of males in some stingless bee species
Publisher: Wiley
Date: 23-09-2002
DOI: 10.1046/J.1365-294X.2002.01589.X
Abstract: In monogynous hymenopteran societies, the number of mates of a queen strongly influences the potential for conflict between workers and queens over the maternity of males. Queens always 'prefer' their own sons to sons of workers, regardless of queen mating frequency. When a queen mates once, workers are more closely related to, and therefore are expected to prefer, their own sons and then sons of sisters to sons of the queen. However, if effective paternity frequency exceeds 2, workers on average should prefer queen-produced males to males produced by their sisters. We studied the queen mating frequency of seven stingless bee species: the Mexican species Scaptotrigona mexicana, S. pectoralis and the Australian species Austroplebeia symei, Trigona clypearis, T. hockingsi, T. mellipes and T. sapiens. We then determined whether males arise from eggs laid by workers or queens in A. symei, T. clypearis, T. hockingsi and T. mellipes. We show that all seven species investigated are most likely singly mated and that the queen dominates reproduction. This indicates that the queen's mating frequency alone does not determine whether workers or the queen produces the males.
Four quantitative trait loci that influence worker sterility in the honeybee (Apis mellifera)
Publisher: Oxford University Press (OUP)
Date: 07-2008
DOI: 10.1534/GENETICS.108.087270
Abstract: The all-female worker caste of the honeybee (Apis mellifera) is effectively barren in that workers refrain from laying eggs in the presence of a fecund queen. The mechanism by which workers switch off their ovaries in queenright colonies is pheromonally cued, but there is genetically based variation among in iduals: some workers have high thresholds for ovary activation, while for others the response threshold is lower. Genetic variation for threshold response by workers to ovary-suppressing cues is most evident in “anarchist” colonies in which mutant patrilines have a proportion of workers that activate their ovaries and lay eggs, despite the presence of a queen. In this study we use a selected anarchist line to create a backcross queenright colony that segregated for high and low levels of ovary activation. We used 191 informative microsatellite loci, covering all 16 linkage groups to identify QTL for ovary activation and test the hypothesis that anarchy is recessively inherited. We reject this hypothesis, but identify four QTL that together explain ∼25% of the phenotypic variance for ovary activation in our mapping population. They provide the first molecular evidence for the existence of quantitative loci that influence selfish cheating behavior in a social animal.
RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens
Publisher: Springer Science and Business Media LLC
Date: 31-07-2015
The dynamic association between ovariole loss and sterility in adult honeybee workers
Publisher: The Royal Society
Date: 29-03-2017
Abstract: In the social insects, ovary state (the presence or absence of mature oocytes) and ovary size (the number of ovarioles) are often used as proxies for the reproductive capacity of an in idual worker. Ovary size is assumed to be fixed post-eclosion whereas ovary state is demonstrably plastic post-eclosion. Here, we show that in fact ovary size declines as honeybee workers age. This finding is robust across two honeybee species: Apis mellifera and A. cerana . The ovariole loss is likely to be due to the regression of particular ovarioles via programmed cell death. We also provide further support for the observation that honeybee workers with activated ovaries (mature oocytes present) most commonly have five ovarioles rather than a greater or smaller number. This result suggests that workers with more than five ovarioles are unable to physiologically support more than five activated ovarioles and that workers with fewer than five ovarioles are below a threshold necessary for ovary activation. As a worker's ovariole number declines with age, studies on worker ovariole number need to take this plasticity into account.
Nest site selection in the open-nesting honeybee Apis florea
Publisher: Springer Science and Business Media LLC
Date: 05-06-2008
Risk assessment for large African hive beetles (Oplostomus spp.)—a review
Publisher: Springer Science and Business Media LLC
Date: 21-02-2017
Expression of genes related to reproduction and pollen foraging in honey bees (Apis mellifera) narcotized with carbon dioxide
Publisher: Wiley
Date: 07-2010
DOI: 10.1111/J.1365-2583.2010.01003.X
Abstract: It has been proposed that a honey bee (Apis mellifera) worker's preference for foraging for pollen or nectar is modulated by a gene network that was originally involved in regulating the reproductive cycles of an ancestral solitary species. We used carbon dioxide to induce narcosis in queens and workers. This treatment is known to initiate oogenesis in queens, reduce oogenesis in queenless workers and to change worker foraging preference. We then assessed changes in gene expression of genes suspected to be involved in either foraging behaviour or reproduction. We show that some genes change expression in the opposite direction between castes in response to treatment. Our results therefore support the hypothesis that reproductive and foraging traits are causally related in the honey bee.
Preservation and loss of the honey bee (Apis) egg-marking signal across evolutionary time
Publisher: Springer Science and Business Media LLC
Date: 06-03-2007
Mitochondrial sequencing and geometric morphometrics suggest two clades in the Tetragonilla collina (Apidae: Meliponini) population of Thailand
Publisher: Springer Science and Business Media LLC
Date: 02-06-2017
Mitochondrial sequencing reveals five separate origins of 'black' Apis mellifera (hymenoptera: Apidae) in Eastern Australian Commercial colonies
Publisher: Oxford University Press (OUP)
Date: 04-2009
DOI: 10.1603/029.102.0203
Abstract: Establishment of a closed population honey bee, Apis mellifera L. (Hymenoptera: Apidae), breeding program based on 'black' strains has been proposed for eastern Australia. Long-term success of such a program requires a high level of genetic variance. To determine the likely extent of genetic variation available, 50 colonies from 11 different commercial apiaries were sequenced in the mitochondrial cytochrome oxidase I and II intergenic region. Five distinct and novel mitotypes were identified. No colonies were found with the A. mellifera mellifera mitotype, which is often associated with undesirable feral strains. One group of mitotypes was consistent with a caucasica origin, two with carnica, and two with ligustica. The results suggest that there is sufficient genetic ersity to support a breeding program provided all these five sources were pooled.
Caste in Social Insects: Genetic Influences Over Caste Determination
Publisher: Elsevier
Date: 2009
Androgenesis: where males hijack eggs to clone themselves
Publisher: The Royal Society
Date: 19-10-2016
Abstract: Androgenesis is a form of quasi-sexual reproduction in which a male is the sole source of the nuclear genetic material in the embryo. Two types of androgenesis occur in nature. Under the first type, females produce eggs without a nucleus and the embryo develops from the male gamete following fertilization. Evolution of this type of androgenesis is poorly understood as the parent responsible for androgenesis (the mother) gains no benefit from it. Ultimate factors driving the evolution of the second type of androgenesis are better understood. In this case, a zygote is formed between a male and a female gamete, but the female genome is eliminated. When rare, androgenesis with genome elimination is favoured because an androgenesis-determining allele has twice the reproductive success of an allele that determines sexual reproduction. Paradoxically, except in hermaphrodites, a successful androgenetic strain can drive such a male-biased sex ratio that the population goes extinct. This likely explains why androgenesis with genome elimination appears to be rarer than androgenesis via non-nucleate eggs, although both forms are either very rare or remain largely undetected in nature. Nonetheless, some highly invasive species including ants and freshwater clams are androgenetic, for reasons that are largely unexplained. This article is part of the themed issue ‘Weird sex: the underappreciated ersity of sexual reproduction’.
Nest defence in a stingless bee: What causes fighting swarms in Trigona carbonaria (Hymenoptera, Meliponini)?
Publisher: Springer Science and Business Media LLC
Date: 18-07-2008
Molecular basis of sex determination in haplodiploids
Publisher: Elsevier BV
Date: 2004
DOI: 10.1016/J.TREE.2003.11.001
Abstract: Sex in many species of Hymenoptera (ants, bees and wasps) is determined by a single locus that is heterozygous in females and hemizygous in (haploid) males. Beye and colleagues have now cloned the csd locus in the honeybee Apis mellifera and provide functional evidence that this gene is the primary switch in the sex-determination cascade of honeybees and possibly all Hymenoptera.
Viable triploid honey bees (apis mellifera capensis) are reliably produced in the progeny of CO2 narcotised queens
Publisher: Oxford University Press (OUP)
Date: 10-2018
Abstract: The haplodiploid system of sex determination of Hymenoptera acts as an exaptation for species to evolve novel forms of asexual reproduction including thelytoky (clonal offspring of the mother). During normal reproduction in Hymenoptera, three of the four products of meiosis that are present in newly-laid eggs are lost as polar bodies, while the remaining pronucleus either develops as a haploid male or fuses with a sperm nucleus to produce a diploid zygote. In contrast, in thelytokous reproduction, which is uncommon but taxonomically widespread, two of the four products of meiosis fuse, as if one acted as a sperm. Queenless workers of Apis mellifera capensis, a subspecies of honey bee from South Africa, routinely reproduce thelytokously. Unmated A. m. capensis queens can also be induced to lay thelytokously by narcosis with carbon dioxide, but mated queens are never thelytokous. We artificially inseminated A. m. capensis queens using CO2 narcosis. Up to 1/3 of offspring workers carried two maternal alleles and an allele of one father whereas no three-allele progeny were seen in control queens of the arrhenotokous (unfertilized eggs result in males) subspecies A. m. scutellata. Flow cytometry of three-allele in iduals revealed that they were triploid and arose from the fertilization of a thelytokous fusion nucleus. We then reared six queens from a narcotized A. m. capensis queen and determined the ploidy of the offspring queens based on microsatellites. One of the five daughters was triploid. Following artificial insemination, this queen produced unfertilized thelytokous diploid eggs at high frequency, and unfertilized triploid eggs at much lower frequency. If fertilized, thelytokous diploid eggs were non-viable, even though triploidy in itself does not impede normal development. In contrast, when the rarer triploid eggs were fertilized, a proportion developed into viable tetraploids. Our study highlights the extraordinary developmental flexibility of haplo-diploid systems.
Size breeds success: Multiple paternity, multivariate selection and male semelparity in a small marsupial, Antechinus stuartii
Publisher: Wiley
Date: 14-08-2006
A quantitative study of worker reproduction in queenright colonies of the Cape honey bee,Apis mellifera capensis
Publisher: Wiley
Date: 06-2009
How does epigenetics influence the course of evolution?
Publisher: The Royal Society
Date: 19-04-2021
Abstract: Epigenetics is the study of changes in gene activity that can be transmitted through cell isions but cannot be explained by changes in the DNA sequence. Epigenetic mechanisms are central to gene regulation, phenotypic plasticity, development and the preservation of genome integrity. Epigenetic mechanisms are often held to make a minor contribution to evolutionary change because epigenetic states are typically erased and reset at every generation, and are therefore, not heritable. Nonetheless, there is growing appreciation that epigenetic variation makes direct and indirect contributions to evolutionary processes. First, some epigenetic states are transmitted intergenerationally and affect the phenotype of offspring. Moreover, bona fide heritable ‘epialleles' exist and are quite common in plants. Such epialleles could, therefore, be subject to natural selection in the same way as conventional DNA sequence-based alleles. Second, epigenetic variation enhances phenotypic plasticity and phenotypic variance and thus can modulate the effect of natural selection on sequence-based genetic variation. Third, given that phenotypic plasticity is central to the adaptability of organisms, epigenetic mechanisms that generate plasticity and acclimation are important to consider in evolutionary theory. Fourth, some genes are under selection to be ‘imprinted' identifying the sex of the parent from which they were derived, leading to parent-of-origin-dependent gene expression and effects. These effects can generate hybrid disfunction and contribute to speciation. Finally, epigenetic processes, particularly DNA methylation, contribute directly to DNA sequence evolution, because they act as mutagens on the one hand and modulate genome stability on the other by keeping transposable elements in check. This article is part of the theme issue ‘How does epigenetics influence the course of evolution?'
Apis florea and Apis cerana workers do not discriminate between queen-laid and worker-laid Apis mellifera eggs
Publisher: Springer Science and Business Media LLC
Date: 08-2019
A scientific note on a rapid method for the molecular discrimination of Apis andreniformis and A. florea
Publisher: Springer Science and Business Media LLC
Date: 16-11-2010
Adaptive, caste-specific changes to recombination rates in a thelytokous honeybee population
Publisher: The Royal Society
Date: 09-06-2021
Abstract: The ability to clone oneself has clear benefits—no need for mate hunting or dilution of one's genome in offspring. It is therefore unsurprising that some populations of haplo-diploid social insects have evolved thelytokous parthenogenesis—the virgin birth of a female. But thelytokous parthenogenesis has a downside: the loss of heterozygosity (LoH) as a consequence of genetic recombination. LoH in haplo-diploid insects can be highly deleterious because female sex determination often relies on heterozygosity at sex-determining loci. The two female castes of the Cape honeybee, Apis mellifera capensis , differ in their mode of reproduction. While workers always reproduce thelytokously, queens always mate and reproduce sexually. For workers, it is important to reduce the frequency of recombination so as to not produce offspring that are homozygous. Here, we ask whether recombination rates differ between Cape workers and Cape queens that we experimentally manipulated to reproduce thelytokously. We tested our hypothesis that Cape workers have evolved mechanisms that restrain genetic recombination, whereas queens have no need for such mechanisms because they reproduce sexually. Using a combination of microsatellite genotyping and whole-genome sequencing we find that a reduction in recombination is confined to workers only.
Evolution: A Royal Seal for Wasp Eggs
Publisher: Elsevier BV
Date: 06-2015
DOI: 10.1016/J.CUB.2015.04.045
Abstract: In many social insects, the queen's reproductive primacy is enforced by policing. If a worker lays an egg, police workers eat it. They spare queen-laid eggs because they are marked with a royal scent, now identified in a wasp.
The 'I see you' prey-predator signal of Apis cerana is innate
Publisher: Springer Science and Business Media LLC
Date: 30-01-2013
DOI: 10.1007/S00114-013-1019-4
Abstract: An 'I see you' (ISY) prey-predator signal can co-evolve when such a signal benefits both prey and predator. The prey benefits if, by producing the signal, the predator is likely to break off an attack. The predator benefits if it is informed by the signal that the prey is aware of its presence and can break off what is likely to be an unsuccessful and potentially costly hunt. Because the signal and response co-evolve in two species, the behaviour underlying an ISY signal is expected to have a strong genetic component and cannot be entirely learned. An ex le of an ISY signal is the 'shimmering' behaviour performed by Asian hive bee workers in the presence of their predator Vespa velutina. To test the prediction that bee-hornet signalling is heritable, we let honey bee workers of two species emerge in an incubator so that they had never been exposed to V. velutina. In Apis cerana, the shimmering response developed 48 h post-emergence, was strong after 72 h and increased further over 2 weeks. In contrast, A. mellifera, which has evolved in the absence of Asian hornets, did not produce the shimmering signal. In control tests, A. cerana workers exposed to a non-threatening butterfly did not respond with the shimmering signal.
The role of epigenetics, particularly DNA methylation, in the evolution of caste in insect societies
Publisher: The Royal Society
Date: 19-04-2021
Abstract: Eusocial insects can be defined as those that live in colonies and have distinct queens and workers. For most species, queens and workers arise from a common genome, and so caste-specific developmental trajectories must arise from epigenetic processes. In this review, we examine the epigenetic mechanisms that may be involved in the regulation of caste dimorphism. Early work on honeybees suggested that DNA methylation plays a causal role in the ergent development of queen and worker castes. This view has now been challenged by studies that did not find consistent associations between methylation and caste in honeybees and other species. Evidence for the involvement of methylation in modulating behaviour of adult workers is also inconsistent. Thus, the functional significance of DNA methylation in social insects remains equivocal. This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’
Responses to Varroa destructor and Nosema ceranae by several commercial strains of Australian and North American honeybees (Hymenoptera: Apidae)
Publisher: Wiley
Date: 14-11-2013
DOI: 10.1111/AEN.12003
Levels of polyandry in Apis laboriosa Smith from Nepal
Publisher: Springer Science and Business Media LLC
Date: 08-2004
Remarkable uniformity in the densities of feral honey bee Apis mellifera Linnaeus, 1758 (Hymenoptera: Apidae) colonies in South Eastern Australia
Publisher: Wiley
Date: 03-04-2014
DOI: 10.1111/AEN.12085
Entomology: A Bee Farming a Fungus
Publisher: Elsevier BV
Date: 11-2015
DOI: 10.1016/J.CUB.2015.09.062
Abstract: Farming is done not only by humans, but also by some ant, beetle and termite species. With the discovery of a stingless bee farming a fungus that provides benefits to its larvae, bees can be added to this list.
No evidence of queen thelytoky following interspecific crosses of the honey bees Apis cerana and Apis mellifera
Publisher: Springer Science and Business Media LLC
Date: 03-02-2017
Workers' sons rescue genetic diversity at the sex locus in an invasive honey bee population
Publisher: Wiley
Date: 04-2019
DOI: 10.1111/MEC.15031
Abstract: The hallmark of eusociality is the ision of labour between reproductive (queen) and nonreproductive (worker) females. Yet in many eusocial insects, workers retain the ability to produce haploid male offspring from unfertilized eggs. The reproductive potential of workers has well-documented consequences for the structure and function of insect colonies, but its implications at the population level are less often considered. We show that worker reproduction in honey bees can have an important role in maintaining genetic ersity at the sex locus in invasive populations. The honey bee sex locus is homozygous-lethal, and, all else being equal, a higher allele number in the population lead to higher mean brood survival. In an invasive population of the honey bee Apis cerana in Australia, workers contribute significantly to male production: 38% of male-producing colonies are queenless, and these contribute one-third of all males at mating congregations. Using a model, we show that such male production by queenless workers will increase the number of sex alleles retained in nascent invasive populations following founder events, relative to a scenario in which only queens reproduce. We conclude that by rescuing sex locus ersity that would otherwise be lost, workers' sons help honey bee populations to minimize the negative effects of inbreeding after founder events and so contribute to their success as invaders.
Queen pheromone modulates the expression of epigenetic modifier genes in the brain of honeybee workers
Publisher: The Royal Society
Date: 12-2020
Abstract: Pheromones are used by many insects to mediate social interactions. In the highly eusocial honeybee ( Apis mellifera ), queen mandibular pheromone (QMP) is involved in the regulation of the reproductive and other behaviour of workers. The molecular mechanisms by which QMP acts are largely unknown. Here, we investigate how genes responsible for epigenetic modifications to DNA, RNA and histones respond to the presence of QMP in the environment. We show that several of these genes are upregulated in the honeybee brain when workers are exposed to artificial QMP. We propose that pheromonal communication systems, such as those used by social insects, evolved to respond to environmental signals by making use of existing epigenomic machineries.
Genome-wide analysis of genes related to ovary activation in worker honey bees
Publisher: Wiley
Date: 06-11-2008
DOI: 10.1111/J.1365-2583.2008.00838.X
Abstract: A defining characteristic of eusocial animals is their ision of labour into reproductive and nonreproductive specialists. Here, we used a microarray study to identify genes associated with functional sterility in the worker honey bee Apis mellifera. We contrasted gene expression in workers from a functionally sterile wild-type strain with that in a mutant (anarchist) strain selected for high rates of ovary activation. We identified a small set of genes from the brain (n = 7) and from the abdomen (n = 5) that are correlated in their expression with early stages of ovary activation. Sterile wild-type workers up-regulated two unknown genes and a homologue of Drosophila CG6004. By contrast, reproductive anarchist workers up-regulated genes for the yolk protein vitellogenin, venom peptides and a member of the AdoHycase superfamily, among others. The differentially expressed genes identified are likely to be involved in early differentiation into sterile and reproductive worker phenotypes and may therefore form part of the gene networks associated with the regulation of honey bee worker sterility. Our study may have lacked sufficient power to detect all but a minority of biologically relevant changes taking place however, the differential expression of vitellogenin and a putative AdoHycase suggests that our screen has captured core reproductive genes and that ovary activation may involve an epigenetic mechanism.
Inheritance of Traits Associated with Reproductive Potential in Apis mellifera capensis and Apis mellifera scutellata Workers
Publisher: Oxford University Press (OUP)
Date: 28-02-2008
Abstract: When workers of the thelytokous Cape honeybee, Apis mellifera capensis, come into contact with colonies of the neighboring arrhenotokous subspecies Apis mellifera scutellata, they can become lethal social parasites. We examined the inheritance of 3 traits (number of ovarioles, number of basitarsal hairs, and size of spermatheca) that are thought to be associated with reproductive potential in A. m. capensis workers. To do so, we produced hybrid A. m. scutellata/A. m. capensis queens and backcrossed them to either A. m. capensis or A. m. scutellata drones. We then measured the 3 traits in parental, hybrid, and backcross offspring. We show that the 3 traits are phenotypically correlated. We also show that the expression of ovariole number, basitarsal hairs, and size of spermatheca is influenced by the genotype of the in idual and the rearing environment but that the influence of the rearing environment is less important to the number of ovarioles. We hypothesize a single recessive allele (l), present at high frequency in natural A. m. capensis populations, which when homozygous causes larvae to elicit more food. This increased feeding as larvae causes resulting adult workers to develop more queen-like morphology and increased reproductive potential. The number of ovarioles, in contrast, appears to be under independent genetic control.
Actual reproductive conflict during emergency queen rearing in Apis florea
Publisher: Springer Science and Business Media LLC
Date: 03-2011
Differences in foraging and broodnest temperature in the honey bees Apis cerana and A. mellifera
Publisher: Springer Science and Business Media LLC
Date: 05-04-2012
Cytogenetic basis of thelytoky in Apis mellifera capensis
Publisher: Springer Science and Business Media LLC
Date: 05-05-2017
A long non-coding RNA is a key factor in the evolution of insect eusociality
Publisher: Cold Spring Harbor Laboratory
Date: 11-05-2022
DOI: 10.1101/2022.05.10.491402
Abstract: Insect sociality is a major evolutionary transition based on the suppression of worker reproduction in favor of the reproductive monopoly of the queen. In the honey bee ( Apis mellifera ) model organism, the development of the two female caste phenotypes, queen and worker, is triggered by differences in their larval diets. However, the mechanistic details underlying their respective developmental trajectories, as well as the maintenance of sterility in the adult workers, are still not fully understood. Here we show that the long non-coding RNA lncov1 interacts with the Tudor staphylococcus nuclease (Tudor-SN) protein to form a regulatory module that promotes apoptosis in the ovaries of worker larvae. In adult workers, the lncov1 /Tudor-SN module responds positively to environmental cues that suppress reproductive capacity. As lncov1 is considerably conserved in the Apidae, we propose that, by promoting worker sterility, the lncov1 /Tudor-SN module has likely played critical roles in the social evolution of bees.
The dynamic DNA methylation cycle from egg to sperm in the honey bee Apis mellifera
Publisher: The Company of Biologists
Date: 07-2014
DOI: 10.1242/DEV.110163
Abstract: In honey bees (Apis mellifera), the epigenetic mark of DNA methylation is central to the developmental regulation of caste differentiation, but may also be involved in additional biological functions. In this study, we examine the whole genome methylation profiles of three stages of the haploid honey bee genome: unfertilised eggs, the adult drones that develop from these eggs and the sperm produced by these drones. These methylomes reveal distinct patterns of methylation. Eggs and sperm show 381 genes with significantly different CpG methylation patterns, with the vast majority being more methylated in eggs. Adult drones show greatly reduced levels of methylation across the genome when compared with both gamete s les. This suggests a dynamic cycle of methylation loss and gain through the development of the drone and during spermatogenesis. Although fluxes in methylation during embryogenesis may account for some of the differentially methylated sites, the distinct methylation patterns at some genes suggest parent-specific epigenetic marking in the gametes. Extensive germ line methylation of some genes possibly explains the lower-than-expected frequency of CpG sites in these genes. We discuss the potential developmental and evolutionary implications of methylation in eggs and sperm in this eusocial insect species.
Higher removal rate of eggs laid by anarchistic queens - A cost of anarchy?
Publisher: Springer Science and Business Media LLC
Date: 30-05-2007
Complete Structure of an Epithelial Keratin Dimer: Implications for Intermediate Filament Assembly
Publisher: Public Library of Science (PLoS)
Date: 16-07-2015
Cheating workers with large activated ovaries avoid risky foraging
Publisher: Oxford University Press (OUP)
Date: 22-03-2014
Nest architecture and genetic differentiation in a species complex of Australian stingless bees
Publisher: Wiley
Date: 06-07-2004
No evidence that habitat disturbance affects mating frequency in the giant honey bee Apis dorsata
Publisher: Springer Science and Business Media LLC
Date: 21-06-2012
Social evolution: Policing without genetic conflict
Publisher: Elsevier BV
Date: 03-2013
DOI: 10.1016/J.CUB.2013.01.051
Abstract: Insect societies have evolved ways of policing selfish behaviour that arises due to genetic conflicts within the colony. A new case of policing in an ant where colony members are genetically identical highlights the role of colony economics for policing.
Evaluating alternative hypotheses for the origin of eusociality in corbiculate bees
Publisher: Elsevier BV
Date: 11-2004
Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): Further support for the parasite/pathogen hypothesis for the evolution of polyandry
Publisher: Springer Science and Business Media LLC
Date: 06-2003
DOI: 10.1007/S00114-003-0418-3
Abstract: Explanations for the evolution of multiple mating by social insect (particularly honey bee) queens have been frequently sought. An important hypothesis is that multiple mating is adaptive because it increases intracolonial genetic ersity and thereby reduces the likelihood that parasites or pathogens will catastrophically infect a colony. We tested one assumption of this model: that honey bee worker patrilines should differ in disease resistance. We used American foulbrood (caused by the bacterium Paenibacillus larvae) as a model pathogen. We found that patrilines within colonies do indeed vary in their resistance to this disease.
Conflict and major transitions — why we need true queens
Publisher: Elsevier BV
Date: 08-2019
DOI: 10.1016/J.COIS.2019.03.009
Abstract: In contrast to human societies, where kings and queens can be sources of conflict, we argue that the morphologically distinct queens of insect colonies are central to the minimization of conflict within their societies. Thus, the evolution of irreversible queen and worker castes represents a major transition in social evolution. Queens are selected to become better reproducers, and workers are selected to become better workers. The reproductive success of queens and workers are, therefore, inextricably linked. Workers achieve reproductive success by assisting the queen, whereas the queen needs her workers to provide her with the wherewithal to raise her brood. The tighter the mutual dependence, the lower conflict, and the larger insect societies can become. As the queen becomes a better breeder, workers are selected to become better at raising their siblings. Yet, nothing in nature is ever free of conflict and with the evolution of a true worker caste a new set of conflicts arises. Multiple mating by queens in particular opens the door to a new set of conflicts. Ironically, multiple mating can only evolve once within-colony conflict is reduced by evolving a true worker caste.
Nest Thermoregulation in Social Insects
Publisher: Elsevier
Date: 2006
Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera)
Publisher: Wiley
Date: 19-03-2010
Intergenerational transfer of DNA methylation marks in the honey bee
Publisher: Proceedings of the National Academy of Sciences
Date: 30-11-2020
Abstract: Intergenerational epigenetic inheritance is usually considered to be of minor significance in mammals because the epigenome is reprogrammed twice between each generation. Yet whether this paradigm holds in nonmammalian organisms is largely unknown. Here, we show that epigenetic marks are transferred across generations in an invertebrate, the honey bee. We found that the epigenome is much more similar between fathers and daughters than between unrelated males and females of different generations within each colony. Epigenetic marks are not only conserved across generations, but also across somatic and germline tissues. Epigenetic reprogramming may thus be a mammalian-specific feature, suggesting a heightened capacity for epigenetic marks to influence evolutionary adaptation across the tree of life.
The ecological impact of commercial beehives on invasive cane toads (Rhinella marina) in eastern Australia
Publisher: Springer Science and Business Media LLC
Date: 12-2017
How does a swarm of the giant Asian honeybee 'Apis dorsata' reach consensus? A study of the individual behaviour of scout bees
Publisher: Springer Science and Business Media LLC
Date: 19-03-2016
Effects of natural mating and CO2 narcosis on biogenic amine receptor gene expression in the ovaries and brain of queen honey bees, Apis mellifera
Publisher: Wiley
Date: 18-09-2012
DOI: 10.1111/J.1365-2583.2012.01159.X
Abstract: A queen honey bee mates at ∼6 days of age, storing the sperm in her spermatheca for life. Mating is associated with profound changes in the behaviour and physiology of the queen but the mechanisms underlying these changes are poorly understood. What is known is that the presence of semen in the oviducts and spermatheca is insufficient to initiate laying, and that copulation or CO(2) narcosis is necessary for ovary activation. In this study we use real-time quantitative PCR to investigate the expression of biogenic amine receptor genes in the brain and ovarian tissue of queens in relation to their reproductive status. We show that dopamine, octopamine and serotonin receptor genes are expressed in the ovaries of queens, and that natural mating, CO(2) narcosis, and the presence of semen in the spermatheca differentially affect their expression. We suggest that these changes may be central to the hormonal cascades that are necessary to initiate oogenesis.
Comb Architecture of the Eusocial Bees Arises from Simple Rules Used During Cell Building
Publisher: Elsevier
Date: 2015
Similar policing rates of eggs laid by virgin and mated honey-bee queens
Publisher: Springer Science and Business Media LLC
Date: 21-10-2004
DOI: 10.1007/S00114-004-0576-Y
Abstract: Worker-policing is a well-documented mechanism that maintains functional worker sterility in queen-right honey-bee colonies. Unknown, however, is the source of the egg-marking signal that is thought to be produced by the queen and used by policing workers to discriminate between queen- and worker-laid eggs. Here we investigate whether mating is necessary for the queen to produce the egg-marking signal. We compare the removal rate of eggs laid by virgin queens and compare this rate with that of eggs laid by mated queens. Our results show that mating does not affect the acceptability of eggs, suggesting that physiological changes linked to the act of mating do not play a role in the production of the queen's egg-marking signal.
Sticking to their choice - Honey bee subfamilies abandon declining food sources at a slow but uniform rate
Publisher: Wiley
Date: 26-03-2003
The density of feral honey bee (Apis mellifera) colonies in South East Australia is greater in undisturbed than in disturbed habitats
Publisher: Springer Science and Business Media LLC
Date: 28-01-2015
Inbred and outbred honey bees (Apis mellifera) have similar innate immune responses
Publisher: Springer Science and Business Media LLC
Date: 27-11-2013
The role of genetic diversity in nest cooling in a wild honey bee, Apis florea
Publisher: Springer Science and Business Media LLC
Date: 30-09-2007
DOI: 10.1007/S00359-006-0176-8
Abstract: Simulation studies of the task threshold model for task allocation in social insect colonies suggest that nest temperature homeostasis is enhanced if workers have slightly different thresholds for engaging in tasks related to nest thermoregulation. Genetic variance in task thresholds is one way a distribution of task thresholds can be generated. Apis mellifera colonies with large genetic ersity are able to maintain more stable brood nest temperatures than colonies that are genetically uniform. If this phenomenon is generalizable to other species, we would predict that patrilines should vary in the threshold in which they engage in thermoregulatory tasks. We exposed A. florea colonies to different temperatures experimentally, and retrieved fanning workers at these different temperatures. In many cases we found statistically significant differences in the proportion of fanning workers of different patrilines at different experimental temperatures. This suggests that genetically different workers have different thresholds for performing the thermoregulatory task of fanning. We suggest, therefore, that genetically based variance in task threshold is a widespread phenomenon in the genus Apis.
No worker reproduction in the Australian stingless bee Trigona carbonaria Smith (Hymenoptera, Apidae)
Publisher: Springer Science and Business Media LLC
Date: 24-04-2015
Cheating honeybee workers produce royal offspring
Publisher: The Royal Society
Date: 28-11-2008
Abstract: The Cape bee ( Apis mellifera capensis ) is unique among honeybees in that workers can lay eggs that instead of developing into males develop into females via thelytokous parthenogenesis. We show that this ability allows workers to compete directly with the queen over the production of new queens. Genetic analyses using microsatellites revealed that 23 out of 39 new queens produced by seven colonies were offspring of workers and not the resident queen. Of these, eight were laid by resident workers, but the majority were offspring of parasitic workers from other colonies. The parasites were derived from several clonal lineages that entered the colonies and successfully targeted queen cells for parasitism. Hence, these parasitic workers had the potential to become genetically reincarnated as queens. Of the daughter queens laid by the resident queen, three were produced asexually, suggesting that queens can ‘choose’ to produce daughter queens clonally and thus have the potential for genetic immortality.
Effects of selection for honey bee worker reproduction on foraging traits
Publisher: Public Library of Science (PLoS)
Date: 04-03-2008
Preferences and tradeoffs in nectar temperature and nectar concentration in the Asian hive bee Apis cerana
Publisher: Springer Science and Business Media LLC
Date: 15-08-2014
Vitellogenin expression in the ovaries of adult honeybee workers provides insights into the evolution of reproductive and social traits
Publisher: Wiley
Date: 20-01-2021
DOI: 10.1111/IMB.12694
Anarchy is a molecular signature of worker sterility in the honey bee
Publisher: Oxford University Press (OUP)
Date: 28-09-2016
Abstract: Worker sterility is a defining characteristic of eusociality. The existence of the sterile worker caste remains a fundamental question for evolutionary biology as it requires the existence of genes that reduce personal reproduction. Currently, little is known about the proximate mechanisms underpinning worker sterility. Studies into a mutant "anarchistic" strain (in which workers can activate their ovaries) of honey bee, Apis mellifera, identified a list of candidate genes that regulate ovary activation. We quantified the expression of the four most promising candidate genes (Anarchy, Pdk1, S6k, and Ulk3) in nonactivated and activated ovaries of wild-type workers. Ovarian expression of Anarchy, a peroxisomal membrane protein, predicts the ovary state of workers with 88.2% accuracy. Increased expression of Anarchy in the ovary is strongly associated with suppression of oogenesis and its expression is sensitive to the presence of the queen. Therefore, Anarchy satisfies key criteria for a "gene underlying altruism". When we knocked down expression of Anarchy in the ovary using RNA interference (RNAi) we altered the expression of Buffy, a gene that regulates programmed cell death. Whole-mount multiplex fluorescent in situ hybridization (mFISH) shows Anarchy transcripts localize to degenerating oocytes within the ovary. Our results suggest that Anarchy is involved in the regulation of oogenesis through programmed cell death. The evolution of facultative worker sterility most likely occurred when the conserved mechanism of programmed cell death was co-opted to regulate ovary activation. Anarchy may therefore be the first ex le of a gene that has evolved through kin selection to regulate worker sterility.
The XVIIth International Conference, Cairns Australia
Publisher: Springer Science and Business Media LLC
Date: 21-12-2014
Variable virulence among isolates of Ascosphaera apis: Testing the parasite-pathogen hypothesis for the evolution of polyandry in social insects
Publisher: Springer Science and Business Media LLC
Date: 23-01-2013
DOI: 10.1007/S00114-013-1016-7
Abstract: The queens of many eusocial insect species are polyandrous. The evolution of polyandry from ancestral monoandry is intriguing because polyandry undermines the kin-selected benefits of high intracolonial relatedness that are understood to have been central to the evolution of eusociality. An accumulating body of evidence suggests that polyandry evolved from monoandry in part because genetically erse colonies better resist infection by pathogens. However, a core assumption of the "parasite-pathogen hypothesis", that there is variation in virulence among strains of pathogens, remains largely untested in vivo. Here, we demonstrate variation in virulence among isolates of Ascosphaera apis, the causative organism of chalkbrood disease in its honey bee (Apis mellifera) host. More importantly, we show a pathogen-host genotypic interaction for resistance and pathogenicity. Our findings therefore support the parasite-parasite hypothesis as a factor in the evolution of polyandry among eusocial insects.
DNA methylation is not a driver of gene expression reprogramming in young honey bee workers
Publisher: Cold Spring Harbor Laboratory
Date: 12-03-2021
DOI: 10.1101/2021.03.12.435154
Abstract: Intragenic DNA methylation, also called gene body methylation, is an evolutionarily-conserved epigenetic mechanism in animals and plants. In social insects, gene body methylation is thought to contribute to behavioral plasticity, for ex le between foragers and nurse workers, by modulating gene expression. However, recent studies have suggested that the majority of DNA methylation is sequence-specific, and therefore cannot act as a flexible mediator between environmental cues and gene expression. To address this paradox, we examined whole-genome methylation patterns in the brains and ovaries of young honey bee workers that had been subjected to ergent social contexts: the presence or absence of the queen. Although these social contexts are known to bring about extreme changes in behavioral and reproductive traits through differential gene expression, we found no significant differences between the methylomes of workers from queenright and queenless colonies. In contrast, thousands of regions were differentially methylated between colonies, and these differences were not associated with differential gene expression in a subset of genes examined. Methylation patterns were highly similar between brain and ovary tissues and only differed in nine regions. These results strongly indicate that DNA methylation is not a driver of differential gene expression between tissues or behavioral morphs. Finally, despite the lack of difference in methylation patterns, queen presence affected the expression of all four DNA methyltransferase genes, suggesting that these enzymes have roles beyond DNA methylation. Therefore, the functional role of DNA methylation in social insect genomes remains an open question.
Assessing the density of honey bee colonies at ecosystem scales
Publisher: Wiley
Date: 23-12-2019
DOI: 10.1111/EEN.12715
A parent-of-origin effect on honeybee worker ovary size
Publisher: The Royal Society
Date: 22-01-2013
Abstract: Apis mellifera capensis is unique among honeybees in that unmated workers can produce pseudo-clonal female offspring via thelytokous parthenogenesis. Workers use this ability to compete among themselves and with their queen to be the mother of new queens. Males could therefore enhance their reproductive success by imprinting genes that enhance fertility in their daughter workers. This possibility sets the scene for intragenomic conflict between queens and drones over worker reproductive traits. Here, we show a strong parent-of-origin effect for ovary size (number of ovarioles) in reciprocal crosses between two honeybee subspecies, A. m. capensis and Apis mellifera scutellata. In this cross, workers with an A. m. capensis father had 30% more ovarioles than genotypically matched workers with an A. m. scutellata father. Other traits we measured (worker weight at emergence and the presence/absence of a spermatheca) are influenced more by rearing conditions than by parent-of-origin effects. Our study is the first to show a strong epigenetic (or, less likely, cytoplasmic maternal) effect for a reproductive trait in the honeybee and suggests that a search for parent-of-origin effects in other social insects may be fruitful.
Whole-Genome DNA Methylation Profile of the Jewel Wasp (Nasonia vitripennis)
Publisher: Oxford University Press (OUP)
Date: 03-2014
Abstract: The epigenetic mark of DNA methylation, the addition of a methyl (CH3) group to a cytosine residue, has been extensively studied in many mammalian genomes and, although it is commonly found at the promoter regions of genes, it is also involved in a number of different biological functions. In other complex animals, such as social insects, DNA methylation has been determined to be involved in caste differentiation and to occur primarily in gene bodies. The role of methylation in nonsocial insects, however, has not yet been explored thoroughly. Here, we present the whole-genome DNA methylation profile of the nonsocial hymenopteran, the jewel wasp (Nasonia vitripennis). From high-throughput sequencing of bisulfite-converted gDNA extracted from male Nasonia thoraces, we were able to determine which cytosine residues are methylated in the entire genome. We found that an overwhelming majority of methylated sites (99.7%) occur at cytosines followed by a guanine in the 3′ direction (CpG sites). Additionally, we found that a majority of methylation in Nasonia occurs within exonic regions of the genome (more than 62%). Overall, methylation is sparse in Nasonia, occurring only at 0.18% of all sites and at 0.63% of CpGs. Our analysis of the Nasonia methylome revealed that in contrast to the methylation profile typically seen in mammals, methylation is sparse and is constrained primarily to exons. This methylation profile is more similar to that of the social hymenopteran species, the honey bee (Apis mellifera). In presenting the Nasonia methylome, we hope to promote future investigation of the regulatory function of DNA methylation in both social and nonsocial hymenoptera.
Paternal effects on Apis mellifera capensis worker ovary size
Publisher: Springer Science and Business Media LLC
Date: 08-05-2017
Thelytokous Parthenogenesis in Unmated Queen Honeybees (Apis mellifera capensis): Central Fusion and High Recombination Rates
Publisher: Oxford University Press (OUP)
Date: 09-2008
DOI: 10.1534/GENETICS.108.090415
Abstract: The subspecies of honeybee indigenous to the Cape region of South Africa, Apis mellifera capensis, is unique because a high proportion of unmated workers can lay eggs that develop into females via thelytokous parthenogenesis involving central fusion of meiotic products. This ability allows pseudoclonal lineages of workers to establish, which are presently widespread as reproductive parasites within the honeybee populations of South Africa. Successful long-term propagation of a parthenogen requires the maintenance of heterozygosity at the sex locus, which in honeybees must be heterozygous for the expression of female traits. Thus, in successful lineages of parasitic workers, recombination events are reduced by an order of magnitude relative to meiosis in queens of other honeybee subspecies. Here we show that in unmated A. m. capensis queens treated to induce oviposition, no such reduction in recombination occurs, indicating that thelytoky and reduced recombination are not controlled by the same gene. Our virgin queens were able to lay both arrhenotokous male-producing haploid eggs and thelytokous female-producing diploid eggs at the same time, with evidence that they have some voluntary control over which kind of egg was laid. If so, they are able to influence the kind of second- ision meiosis that occurs in their eggs post partum.
Genetic structure of nest aggregations and drone congregations of the southeast Asian stingless bee Trigona collina
Publisher: Wiley
Date: 16-06-2004
Reproductive interference between honeybee species in artificial sympatry
Publisher: Wiley
Date: 24-02-2014
DOI: 10.1111/MEC.12669
Abstract: Reproductive isolation between closely related species is often incomplete. The Western honeybee, Apis mellifera, and the Eastern hive bee, Apis cerana, have been allopatric for millions of years, but are nonetheless similar in morphology and behaviour. During the last century, the two species were brought into contact anthropogenically, providing potential opportunities for interspecific matings. Hybrids between A. mellifera and A. cerana are inviable, so natural interspecific matings are of concern because they may reduce the viability of A. cerana and A. mellifera populations - two of the world's most important pollinators. We examined the mating behaviour of A. mellifera and A. cerana queens and drones from Caoba Basin, China and Cairns, Australia. Drone mating flight times overlap in both areas. Analysis of the spermathecal contents of queens with species-specific genetic markers indicated that in Caoba Basin, 14% of A. mellifera queens mated with at least one A. cerana male, but we detected no A. cerana queens that had mated with A. mellifera males. Similarly, in Cairns, no A. cerana queens carried A. mellifera sperm, but one-third of A. mellifera queens had mated with at least one A. cerana male. No hybrid embryos were detected in eggs laid by interspecifically mated A. mellifera queens in either location. However, A. mellifera queens artificially inseminated with A. cerana sperm produced inviable hybrid eggs or unfertilized drones. This suggests that reproductive interference will impact the viability of honeybee populations wherever A. cerana and A. mellifera are in contact.
Simulation models of the role of genetic variability in social insect task allocation
Publisher: Springer Science and Business Media LLC
Date: 05-2004
Biogenic amine receptor gene expression in the ovarian tissue of the honey bee Apis mellifera
Publisher: Wiley
Date: 12-09-2012
DOI: 10.1111/J.1365-2583.2011.01106.X
Abstract: In the honey bee Apis mellifera loss of the queen from a colony induces increased levels of the biogenic amine dopamine in the brain of workers, and this elevation is correlated with ovary activation. In the present study we use real-time quantitative PCR to investigate expression of five biogenic amine receptor genes. We show that biogenic amine receptors are expressed in ovarian tissue, and that their expression is strongly influenced by the presence or absence of a queen in the colony. In contrast to the brain, where all three dopamine receptors are expressed, only two dopamine receptors are expressed in the ovaries, and their expression is strongly correlated with the reproductive status of workers. We conclude that biogenic amine receptors are expressed in the ovaries and are likely to be directly influential in the regulation of worker sterility in honey bees.
Parent-of-origin effects on genome-wide DNA methylation in the Cape honey bee (Apis mellifera capensis) may be confounded by allele-specific methylation
Publisher: Springer Science and Business Media LLC
Date: 12-03-2016
Genetic correlation between amyotrophic lateral sclerosis and schizophrenia
Publisher: Springer Science and Business Media LLC
Date: 21-03-2017
DOI: 10.1038/NCOMMS14774
Abstract: We have previously shown higher-than-expected rates of schizophrenia in relatives of patients with amyotrophic lateral sclerosis (ALS), suggesting an aetiological relationship between the diseases. Here, we investigate the genetic relationship between ALS and schizophrenia using genome-wide association study data from over 100,000 unique in iduals. Using linkage disequilibrium score regression, we estimate the genetic correlation between ALS and schizophrenia to be 14.3% (7.05–21.6 P =1 × 10 −4 ) with schizophrenia polygenic risk scores explaining up to 0.12% of the variance in ALS ( P =8.4 × 10 −7 ). A modest increase in comorbidity of ALS and schizophrenia is expected given these findings (odds ratio 1.08–1.26) but this would require very large studies to observe epidemiologically. We identify five potential novel ALS-associated loci using conditional false discovery rate analysis. It is likely that shared neurobiological mechanisms between these two disorders will engender novel hypotheses in future preclinical and clinical studies.
Paternally‐biased gene expression follows kin‐selected predictions in female honey bee embryos
Publisher: Wiley
Date: 04-2020
DOI: 10.1111/MEC.15419
Who is the Queen's mother? Royal cheats in social insects
Publisher: Springer Science and Business Media LLC
Date: 06-2008
Do policing honeybee (Apis mellifera) workers target eggs in drone comb?
Publisher: Springer Science and Business Media LLC
Date: 02-2003
Thermal adaptation in the honeybee (Apis mellifera) via changes to the structure of malate dehydrogenase
Publisher: The Company of Biologists
Date: 2020
DOI: 10.1242/JEB.228239
Abstract: In honeybees there are three alleles of cytosolic malate dehydrogenase: F, M and S. Allele frequencies are correlated with environmental temperature, suggesting that the alleles have temperature-dependent fitness benefits. We determined the enzymic activity of each allele across a range of temperatures in vitro. The F and S alleles have higher activity and are less sensitive to high temperatures than the M allele, which loses activity after incubation at temperatures found in the thorax of foraging bees in hot climates. Next, we predicted the protein structure of each allele and used molecular dynamics simulations to investigate their molecular flexibility. The M allele is more flexible than the S and F alleles at 50°C, suggesting a plausible explanation for M's loss of activity at high temperatures, and has the greatest structural flexibility at 15°C, suggesting that it can retain some enzyme activity at cooler temperatures. MM bees recovered from two hours of cold narcosis significantly better than all other genotypes. Combined, these results explain clinal variation in MDH allele frequencies in the honeybee at the molecular level.
Domestication of honey bees was associated with expansion of genetic diversity
Publisher: Wiley
Date: 09-2012
Global allele polymorphism indicates a high rate of allele genesis at a locus under balancing selection
Publisher: Springer Science and Business Media LLC
Date: 27-08-2020
Genetic structure of island and mainland populations of a Neotropical bumble bee species
Publisher: Springer Science and Business Media LLC
Date: 07-05-2016
Hybridization and asymmetric introgression between Tetragonisca angustula and Tetragonisca fiebrigi
Publisher: Springer Science and Business Media LLC
Date: 02-08-2014
A scientific note on a genetically-determined color morph of the dwarf honey bee, Apis and reniformis,Note scientifique sur un morphe de couleur à détermination génétique chez l’abeille naine, Apis andreniformis,Eine wissenschaftliche Notiz über eine genetisch determinierte Farbvariante der Zwerghonigbiene, Apis andreniformis
Publisher: Springer Science and Business Media LLC
Date: 13-05-2009
A scientific note on the mating frequency of Apis dorsata
Publisher: Springer Science and Business Media LLC
Date: 2003
Strikingly high levels of heterozygosity despite 20 years of inbreeding in a clonal honey bee
Publisher: Wiley
Date: 07-12-2019
DOI: 10.1111/JEB.13397
Abstract: Inbreeding (the mating between closely related in iduals) often has detrimental effects that are associated with loss of heterozygosity at overdominant loci, and the expression of deleterious recessive alleles. However, determining which loci are detrimental when homozygous, and the extent of their phenotypic effects, remains poorly understood. Here, we utilize a unique inbred population of clonal (thelytokous) honey bees, Apis mellifera capensis, to determine which loci reduce in idual fitness when homozygous. This asexual population arose from a single worker ancestor approximately 20 years ago and has persisted for at least 100 generations. Thelytokous parthenogenesis results in a 1/3 of loss of heterozygosity with each generation. Yet, this population retains heterozygosity throughout its genome due to selection against homozygotes. Deep sequencing of one bee from each of the three known sub-lineages of the population revealed that 3,766 of 10,884 genes (34%) have retained heterozygosity across all sub-lineages, suggesting that these genes have heterozygote advantage. The maintenance of heterozygosity in the same genes and genomic regions in all three sub-lineages suggests that nearly every chromosome carries genes that show sufficient heterozygote advantage to be selectively detrimental when homozygous.
Queen signals in a stingless bee: suppression of worker ovary activation and spatial distribution of active compounds
Publisher: Springer Science and Business Media LLC
Date: 12-12-2014
DOI: 10.1038/SREP07449
Genetic Structure of an Apis dorsata Population: The Significance of Migration and Colony Aggregation
Publisher: Oxford University Press (OUP)
Date: 03-2004
Abstract: Eight microsatellite loci were used to investigate the genetic structure of the giant honeybee (Apis dorsata) population in northeast India. This species migrates seasonally between summer and winter nesting sites, and queens appear to return to their previously occupied site. Furthermore, there is a strong tendency for colonies of this species to aggregate at perennially utilized nesting sites that may be shared by more than 150 colonies. These behavioral features suggest that colonies within aggregations should be more related than random colonies, but that the long-distance migration could act to minimize genetic differentiation both between geographical areas and within aggregations. Our genetic study supports these conjectures arising from natural history. A. dorsata aggregations are comprised of colonies that share more alleles than expected by chance. Although queens heading neighboring colonies are not close relatives, fixation indices show significant genetic differentiation among aggregation sites. However, there appears to be sufficient gene flow among aggregations to prevent high degrees of relatedness developing between colonies within aggregations. The results also suggest that there is significant population structuring between geographical regions, although the level of structuring caused by aggregation exceeds the differentiation attributable to geographic region.
Honey bee (Apis mellifera) sperm competition in vitro - Two are no less viable than one
Publisher: Springer Science and Business Media LLC
Date: 09-06-2009
Heritability of worker ovariole number in the cape honey bee apis mellifera capensis
Publisher: Springer Science and Business Media LLC
Date: 07-03-2012
Regulation of oogenesis in honey bee workers via programed cell death
Publisher: Elsevier BV
Date: 10-2015
DOI: 10.1016/J.JINSPHYS.2015.06.014
Abstract: Reproductive ision of labour characterises eusociality. Currently little is known about the mechanisms that underlie the 'sterility' of the worker caste, but queen pheromone plays a major role in regulating the reproductive state. Here we investigate oogenesis in the young adult honey bee worker ovary in the presence of queen pheromone and in its absence. When queen pheromone is absent, workers can activate their ovaries and have well-developed follicles. When queen pheromone is present, even though workers have non-activated ovaries, they continually produce oocytes which are aborted at an early stage. Therefore, irrespective of the presence of the queen, the young adult worker ovary contains oocytes. By this means young workers retain reproductive plasticity. The degeneration of the germ cells in the ovarioles of workers in the presence of queen pheromone has the morphological hallmarks of programmed cell death. Therefore the mechanistic basis of 'worker sterility' relies in part on the regulation of oogenesis via programmed cell death. Our results suggest that honey bees have co-opted a highly conserved checkpoint at mid-oogenesis to regulate the fertility of the worker caste.
Seven suggestive quantitative trait loci influence hygienic behavior of honey bees
Publisher: Springer Science and Business Media LLC
Date: 12-2002
DOI: 10.1007/S00114-002-0371-6
Abstract: In 1964, Walter Rothenbuhler proposed a two-gene model to explain phenotypic variance in the remarkable behavior in which honey bee workers remove dead brood from their colonies. Rothenbuhler's model proposed that one locus controls the uncapping of brood cells containing dead pupae, while a second controls the removal of the cell contents. We show here, through molecular techniques and quantitative trait loci (QTL) linkage mapping, that the genetic basis of hygienic behavior is more complex, and that many genes are likely to contribute to the behavior. In our cross, we detected seven suggestive QTLs associated with hygienic behavior. Each detected QTL controlled only 9-15% of the observed phenotypic variance in the character.
Erratum: (Molecular Ecology (2012))
Publisher: Wiley
Date: 07-02-2013
DOI: 10.1111/MEC.12133
Thelytoky in the honey bee
Publisher: Springer Science and Business Media LLC
Date: 22-01-2014
Consensus building in giant Asian honeybee, 'Apis dorsata', swarms on the move
Publisher: Elsevier BV
Date: 07-2014
Brood comb construction by the stingless bees 'Tetragonula hockingsi' and 'Tetragonula carbonaria'
Publisher: Springer Science and Business Media LLC
Date: 26-04-2012
Sex mosaics in the honeybee: how haplodiploidy makes possible the evolution of novel forms of reproduction in social Hymenoptera
Publisher: The Royal Society
Date: 11-2018
Abstract: Hymenoptera are haplodiploid: females arise from fertilized, diploid eggs, while males arise from unfertilized, haploid eggs. The cytogenetic mechanisms underlying haplodiploidy enable remarkable phenomena including female cloning, male cloning and gynandromorphy (sex mosaics). We collected 11 newly emerged putative gynandromorph honeybees from a single colony, assessed the sex of various tissues morphologically and determined the genetic origin (maternal or paternal) of each tissue by genotyping. Ten bees were gynandromorphs with one to three distinct paternal origins. Remarkably, one bee carried no maternal alleles. This bee had female organs throughout, and arose from the fusion of two sperm nuclei. This is the first reported case in the Hymenoptera of sperm fusion resulting in a female, emphasizing the flexibility for social insect reproduction and potentially novel colony-level social structures.
Large fitness benefits from polyandry in the honey bee, Apis mellifera
Publisher: Elsevier BV
Date: 02-2008
Retinue attraction and ovary activation: Responses of wild type and anarchistic honey bees (Apis mellifera) to queen and brood pheromones
Publisher: Springer Science and Business Media LLC
Date: 26-08-2005
Phantom alternatives influence food preferences in the eastern honeybee Apis cerana
Publisher: Wiley
Date: 20-10-2015
Abstract: Most models of animal choice behaviour assume that desirable but unavailable options, such as a high quality, but inhabited nest sites, do not influence an in idual's preferences for the remaining options. However, experiments suggest that in mammals, the mere presence of such 'phantom' alternatives can alter, and even reverse, an in idual's preferences for other items in a choice set. Phantom alternatives may be widespread in nature, as they occur whenever a resource is visible, but unavailable at the time of choice. They are particularly relevant for nectar-foraging animals, where previously rewarding flowers may sometimes be empty. Here, we investigate the effect of phantom alternatives on feeder preferences in the eastern honeybee, Apis cerana. First, we tested the effects of unattractive and attractive phantom alternatives by presenting in idual bees with either a binary choice set containing two feeders that differed strongly in two qualities, but were equally preferred overall ('option 1' and 'option 2'), or a ternary choice set containing option 1, option 2 and one of two phantom types (unattractive and attractive). Secondly, we determined whether phantoms increase (similarity effect) or decrease (dissimilarity effect) preference for phantom-similar choices. In binary trials, bees had no significant preference for option 1 or option 2. However, after encountering an attractive phantom alternative, in idual bees preferred option 2. The unattractive phantom did not influence bee preferences. Phantoms consistently changed in idual bee preferences in favour of the phantom-similar choice. This means that the presence of an attractive food source, even if it is unavailable, can influence preference relationships between remaining items in the choice set. Our findings highlight the importance of considering the potential for phantom effects when studying the foraging behaviour of animals. Our results are particularly relevant for nectarivores, where empty but previously rewarding flowers are a common occurrence. Since an increase in pollinator visits can result in higher seed set, our results open up the possibility that by shifting pollinator preferences, empty flowers could have otherwise-unpredicted influences on community composition, plant-pollinator interactions and pollinator behaviour.
Individual honey bee (Apis cerana) foragers adjust their fuel load to match variability in forage reward
Publisher: Springer Science and Business Media LLC
Date: 09-11-2015
DOI: 10.1038/SREP16418
Abstract: Animals may adjust their behavior according to their perception of risk. Here we show that free-flying honey bee ( Apis cerana ) foragers mitigate the risk of starvation in the field when foraging on a food source that offers variable rewards by carrying more ‘fuel’ food on their outward journey. We trained foragers to a feeder located 1.2 km from each of four colonies. On average foragers carried 12.7% greater volume of fuel, equivalent to 30.2% more glucose when foraging on a variable source (a random sequence of 0.5, 1.5 and 2.5 M sucrose solution, average sucrose content 1.5 M) than when forging on a consistent source (constant 1.5 M sucrose solution). Our findings complement an earlier study that showed that foragers decrease their fuel load as they become more familiar with a foraging place. We suggest that honey bee foragers are risk sensitive and carry more fuel to minimize the risk of starvation in the field when a foraging trip is perceived as being risky, either because the forager is unfamiliar with the foraging site, or because the forage available at a familiar site offers variable rewards.
Patterns of Apis mellifera infestation by Nosema ceranae support the parasite hypothesis for the evolution of extreme polyandry in eusocial insects
Publisher: Springer Science and Business Media LLC
Date: 15-02-2012
Lack of interspecific parasitism between the dwarf honeybees Apis andreniformis and Apis florea
Publisher: Springer Science and Business Media LLC
Date: 03-03-2010
Response to reproductive biology of the Cape honeybee: A critique of Beekman et al. by Pirk et al.
Publisher: Oxford University Press (OUP)
Date: 11-05-2012
Morphological and molecular characters reveal differentiation in a Neotropical social bee, Melipona beecheii (Apidae: Meliponini)
Publisher: Springer Science and Business Media LLC
Date: 07-03-2007
Conservation of Asian honey bees
Publisher: Springer Science and Business Media LLC
Date: 05-2009
Egg marking pheromones of anarchistic worker honeybees (Apis mellifera)
Publisher: Oxford University Press (OUP)
Date: 09-2004
Modelling the role of intracolonial genetic diversity on regulation of brood temperature in honey bee (Apis mellifera L.) colonies
Publisher: Springer Science and Business Media LLC
Date: 05-2006
Collective decision making in the red dwarf honeybee Apis florea
Publisher: Springer Science and Business Media LLC
Date: 07-08-2017
Different bees, different needs: how nest-site requirements have shaped the decision-making processes in homeless honeybees ( Apis spp.)
Publisher: The Royal Society
Date: 26-03-2018
Abstract: During reproductive swarming, a honeybee swarm needs to decide on a new nest site and then move to the chosen site collectively. Most studies of swarming and nest-site selection are based on one species, Apis mellifera . Natural colonies of A. mellifera live in tree cavities. The quality of the cavity is critical to the survival of a swarm. Other honeybee species nest in the open, and have less strict nest-site requirements, such as the open-nesting dwarf honeybee Apis florea . Apis florea builds a nest comprised of a single comb suspended from a twig. For a cavity-nesting species, there is only a limited number of potential nest sites that can be located by a swarm, because suitable sites are scarce. By contrast, for an open-nesting species, there is an abundance of equally suitable twigs. While the decision-making process of cavity-nesting bees is geared towards selecting the best site possible, open-nesting species need to coordinate collective movement towards areas with potential nest sites. Here, we argue that the nest-site selection processes of A. florea and A. mellifera have been shaped by each species' specific nest-site requirements. Both species use the same behavioural algorithm, tuned to allow each species to solve their species-specific problem. This article is part of the theme issue ‘Collective movement ecology’.
Phylogenetic and physiological characterization of a heterotrophic, chemolithoautotrophic Thiothrix strain isolated from activated sludge
Publisher: Microbiology Society
Date: 09-2003
Abstract: The sheathed filamentous bacterium known as strain CT3, isolated by micromanipulation from an activated sludge treatment plant in Italy, is a member of the genus Thiothrix in the gamma-Proteobacteria according to 16S rDNA sequence analysis. The closest phylogenetic neighbours of strain CT3 are strains I and Q(T), which were also isolated from activated sludge and belong to the species Thiothrix fructosivorans. These strains have respectively 99.2 and 99.4 % similarity to CT3 by 16S rDNA sequence comparison. CT3 shows 63-67 % DNA-DNA hybridization with strain I, which is the only currently viable strain of T. fructosivorans. CT3 is the second strain in the genus Thiothrix that has been shown to be capable of growing autotrophically with reduced sulfur compounds as the sole energy source autotrophy was also confirmed in strain I. The first reported chemolithoautotrophic isolate of this genus was a strain of 'Thiothrix ramosa' that was isolated from a hydrogen sulfide spring and is morphologically distinguishable from all other described strains of Thiothrix, including CT3. CT3 is an aerobic organism that is non-fermentative, not capable of denitrification and able to grow heterotrophically. Autotrophy in the genus Thiothrix should be investigated more fully to better define the taxonomy of this genus.
Pheromones affecting ovary activation and ovariole loss in the Asian honey bee Apis cerana
Publisher: Elsevier BV
Date: 03-2015
DOI: 10.1016/J.JINSPHYS.2015.01.006
Abstract: The Asian hive bee Apis cerana has similar queen mandibular pheromones (QMP) to the Western honey bee Apismellifera. However the effects of in idual QMP components have never been tested to determine their effects on the reproductive physiology of A. cerana workers. We fed one queen equivalent of each of the major components of A. cerana QMP to groups of c.a. 500 day-old, caged, workers twice a day until the workers were 10 days old. Half of the cages were also provided with 10% royal jelly in the food. Workers were s led each day and dissected to determine the number of ovarioles and the degree of ovary activation (egg development). In cages treated with 9-carbon fatty acids ovary activation was minimal, whereas the 10-carbon acids suppressed ovary activation very little. Royal jelly enhanced ovary activation, especially in cages treated with 10-carbon acids. The number of ovarioles declined with bee age, but the rate of decline was slowed by the 9-carbon acids in particular. The results show conservation of the composition and function of QMP between A. cerana and A. mellifera and support the hypothesis that QMP is an honest signal of queen fecundity rather than a chemical castrator of workers.
Social Parasitism in the Honeybee (Apis mellifera) Is Not Controlled by a Single SNP
Publisher: Oxford University Press (OUP)
Date: 26-04-2019
Abstract: The Cape bee (Apis mellifera capensis) is a subspecies of the honeybee, in which workers commonly lay diploid unfertilized eggs via a process known as thelytoky. A recent study aimed to map the genetic basis of this trait in the progeny of a single capensis queen where workers laid either diploid (thelytokous) or haploid (arrhenotokous) eggs. A nonsynonymous single nucleotide polymorphism (SNP) in a gene of unknown function was reported to be strongly associated with thelytoky in this colony. Here, we analyze genome sequences from a global s le of A. mellifera and identify populations where the proposed thelytoky allele at this SNP is common but thelytoky is absent. We also analyze genome sequences of three capensis queens produced by thelytoky and find that, contrary to predictions, they do not carry the proposed thelytoky allele. The proposed SNP is therefore neither sufficient nor required to produce thelytoky in A. mellifera.
Dance precision of Apis florea - Clues to the evolution of the honeybee dance language?
Publisher: Springer Science and Business Media LLC
Date: 27-02-2008
Differential reproductive success among subfamilies in queenless honeybee (Apis mellifera L.) colonies
Publisher: Springer Science and Business Media LLC
Date: 05-2004
Social Insects: Rearing Temperature Affects Ant Thermoregulatory Behaviour
Publisher: Elsevier BV
Date: 12-2009
DOI: 10.1016/J.CUB.2009.09.038
Abstract: Differing task thresholds among workers are crucial to the efficient allocation of work in self-organized insect colonies. New evidence suggests that the rearing temperature of ant pupae causes lifelong changes in an ant's response threshold to temperature.
Microsatellite loci for laticaudine sea kraits
Publisher: Wiley
Date: 29-08-2008
DOI: 10.1111/J.1755-0998.2008.02227.X
Abstract: We report the development of 11 polymorphic microsatellite loci (three dinucleotides, one trinucleotide and seven tetranucleotides) that are useful for the detection of population sub ision and the study of philopatry, migration and mating biology in laticaudine sea kraits Laticauda saintgironsi and Laticauda laticaudata. Five loci are highly polymorphic and lify reliably in both L. saintgironsi and L. laticaudata. An additional three are useful in L. saintgironsi and another three in L. laticaudata.
Modelling estimates of honey bee (Apis spp.) colony density from drones
Publisher: Elsevier BV
Date: 10-2013
Associations between reproduction and work in workers of the Asian hive bee Apis cerana
Publisher: Elsevier BV
Date: 11-2015
DOI: 10.1016/J.JINSPHYS.2015.08.003
Abstract: If a honey bee (Apis spp.) colony becomes queenless, about 1/3 of young workers activate their ovaries and produce haploid male-producing eggs. In doing so queenless workers maximize their inclusive fitness because the normal option of vicarious production of relatives via their queen's eggs is no longer available. But if many workers are engaged in reproduction, how does a queenless colony continue to feed its brood and forage? Here we show that in the Asian hive bee Apis cerana hypopharyngeal gland (HPG) size is larger in queenless workers than in queenright workers and that bees undertaking brood-rearing tasks have larger HPG than same-aged bees that are foraging. In queenless colonies, workers with a smaller number of ovarioles are more likely to have activated ovaries. This reinforces the puzzling observation that a large number of ovarioles reduces reproductive success in queenless A. cerana. It further suggests that reproductive workers either avoid foraging or transition to foraging later in life than non-reproductive workers. Finally, our study also showed that ovary activation and larger-than-average numbers of ovarioles had no statistically detectable influence on foraging specialization for pollen or nectar.
Honeybee workers use cues other than egg viability for policing
Publisher: The Royal Society
Date: 16-05-2005
Abstract: Worker policing, wherein social insect workers prevent their sisters from reproducing by eating worker-laid eggs, is recognized as a textbook ex le of kin selection in action. However, the evolutionary basis of policing was recently challenged in a study that suggested that police-workers remove worker-laid eggs not because rearing workers' sons reduces worker fitness, but merely because worker-laid eggs have low viability. Here, we refute Pirk et al. 's conclusions. First, we confirm earlier work that showed equal viability of eggs laid by queens and workers. Second, a statistical analysis of the data of Pirk et al. reveals that their own data do not support the conclusion that worker-laid eggs are policed merely because of their low viability. Third, we present data that unequivocally show that police-workers cannot discriminate between dead and live eggs. Hence, our study seriously weakens the challenge to the kin-selected basis of policing in honeybees.
Experimental manipulation of ovary activation and gene expression in honey bee (Apis mellifera) queens and workers: Testing hypotheses of reproductive regulation
Publisher: Wiley
Date: 2007
DOI: 10.1002/JEZ.415
Abstract: A fundamental issue in sociobiology is to understand how social insect females regulate their in idual reproduction to maximize colony and personal fitness. Although the social cues mediating reproductive output within castes of the honey bees (Apis mellifera) are understood at a basic level, the underlying gene regulatory networks are not. In this study, we investigate the expression of 25 genes whose function suggests a role in the gene networks that regulate ovary activation--a functional determinant of reproductive skew. To this end, we used CO2 narcosis to manipulate ovary activation in queens and workers, and then quantified concomitant changes in gene expression using quantitative polymerase chain reaction. Of the 25 genes studied, ten were differentially expressed between treated and control groups in at least one caste. Two of these genes, a ribosomal protein and a tyramine receptor, were differentially expressed between treatments and controls in both castes. We use the expression pattern of all differentially expressed genes to test hypotheses for the caste-specific regulation of ovary activation in honey bees.
Behavioural tactics used by invasive cane toads (Rhinella marina) to exploit apiaries in Australia
Publisher: Wiley
Date: 12-10-2019
DOI: 10.1111/AEC.12668
Do queens select sperm? [1] (multiple letters)
Publisher: Elsevier BV
Date: 03-2003
Moving home: nest-site selection in the Red Dwarf honeybee ('Apis florea')
Publisher: Springer Science and Business Media LLC
Date: 09-11-2011
Behavioural Genetics of the Honey Bee Apis mellifera
Publisher: Elsevier
Date: 2006
An 'I see you' prey-predator signal between the Asian honeybee, Apis cerana, and the hornet, Vespa velutina
Publisher: Elsevier BV
Date: 04-2012
Queen pheromone: Contraceptive or a queen presence signal?—A comment on Holman
Publisher: Oxford University Press (OUP)
Date: 28-04-2018
Erratum: Molecular basis of sex determination in haplodiploids (Trends in Ecology and Evolution)
Publisher: Elsevier BV
Date: 03-2004
Aggregations of unrelated Apis florea colonies
Publisher: Springer Science and Business Media LLC
Date: 09-2008
Parent-of-origin effects, allele-specific expression, genomic imprinting and paternal manipulation in social insects
Publisher: The Royal Society
Date: 19-04-2021
Abstract: Haplo-diploidy and the relatedness asymmetries it generates mean that social insects are prime candidates for the evolution of genomic imprinting. In single-mating social insect species, some genes may be selected to evolve genomic mechanisms that enhance reproduction by workers when they are inherited from a female. This situation reverses in multiple mating species, where genes inherited from fathers can be under selection to enhance the reproductive success of daughters. Reciprocal crosses between subspecies of honeybees have shown strong parent-of-origin effects on worker reproductive phenotypes, and this could be evidence of such genomic imprinting affecting genes related to worker reproduction. It is also possible that social insect fathers directly affect gene expression in their daughters, for ex le, by placing small interfering RNA molecules in semen. Gene expression studies have repeatedly found evidence of parent-specific gene expression in social insects, but it is unclear at this time whether this arises from genomic imprinting, paternal manipulation, an artefact of cyto-nuclear interactions, or all of these. This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’
Related Organisations
Related Funding Activities
Discovery Projects - Grant ID: DP0985189
Start Date: 03-2009
End Date: 12-2012
Amount: $250,000.00
Funder: Australian Research Council
View Funded ActivityLinkage Projects - Grant ID: LP0669286
Start Date: 02-2007
End Date: 06-2011
Amount: $105,000.00
Funder: Australian Research Council
View Funded ActivityDiscovery Projects - Grant ID: DP150100151
Start Date: 2015
End Date: 01-2018
Amount: $424,000.00
Funder: Australian Research Council
View Funded ActivityDiscovery Projects - Grant ID: DP120101915
Start Date: 02-2012
End Date: 12-2015
Amount: $199,000.00
Funder: Australian Research Council
View Funded ActivityLinkage - International - Grant ID: LX0348218
Start Date: 02-2004
End Date: 01-2007
Amount: $30,300.00
Funder: Australian Research Council
View Funded ActivityDiscovery Projects - Grant ID: DP180101696
Start Date: 2018
End Date: 12-2020
Amount: $289,844.00
Funder: Australian Research Council
View Funded ActivityDiscovery Projects - Grant ID: DP150101985
Start Date: 2015
End Date: 01-2018
Amount: $364,700.00
Funder: Australian Research Council
View Funded ActivityDiscovery Projects - Grant ID: DP0878924
Start Date: 01-2008
End Date: 01-2013
Amount: $620,000.00
Funder: Australian Research Council
View Funded ActivityDiscovery Projects - Grant ID: DP0343170
Start Date: 02-2003
End Date: 01-2006
Amount: $560,000.00
Funder: Australian Research Council
View Funded ActivityDiscovery Projects - Grant ID: DP190101500
Start Date: 2019
End Date: 06-2022
Amount: $321,000.00
Funder: Australian Research Council
View Funded ActivityDiscovery Projects - Grant ID: DP210101084
Start Date: 12-2021
End Date: 01-2022
Amount: $288,760.00
Funder: Australian Research Council
View Funded ActivityLinkage Infrastructure, Equipment And Facilities - Grant ID: LE110100134
Start Date: 2011
End Date: 12-2011
Amount: $160,240.00
Funder: Australian Research Council
View Funded ActivityDiscovery Projects - Grant ID: DP0450569
Start Date: 02-2004
End Date: 01-2007
Amount: $600,000.00
Funder: Australian Research Council
View Funded ActivityDiscovery Projects - Grant ID: DP0664629
Start Date: 05-2006
End Date: 05-2009
Amount: $476,000.00
Funder: Australian Research Council
View Funded Activity