Kate Sanders

The evolution of scale sensilla in the transition from land to sea in elapid snakes

Publisher: The Royal Society

Date: 06-2016

DOI: 10.1098/RSOB.160054

Abstract: Scale sensilla are small tactile mechanosensory organs located on the head scales of many squamate reptiles (lizards and snakes). In sea snakes and sea kraits (Elapidae: Hydrophiinae), these scale organs are presumptive scale sensilla that purportedly function as both tactile mechanoreceptors and potentially as hydrodynamic receptors capable of sensing the displacement of water. We combined scanning electron microscopy, silicone casting of the skin and quadrate s ling with a phylogenetic analysis to assess morphological variation in sensilla on the postocular head scale(s) across four terrestrial, 13 fully aquatic and two semi-aquatic species of elapids. Substantial variation exists in the overall coverage of sensilla (0.8–6.5%) among the species s led and is broadly overlapping in aquatic and terrestrial lineages. However, two observations suggest a ergent, possibly hydrodynamic sensory role of sensilla in sea snake and sea krait species. First, scale sensilla are more protruding (dome-shaped) in aquatic species than in their terrestrial counterparts. Second, exceptionally high overall coverage of sensilla is found only in the fully aquatic sea snakes, and this attribute appears to have evolved multiple times within this group. Our quantification of coverage as a proxy for relative ‘sensitivity’ represents the first analysis of the evolution of sensilla in the transition from terrestrial to marine habitats. However, evidence from physiological and behavioural studies is needed to confirm the functional role of scale sensilla in sea snakes and sea kraits.

The sex life aquatic: sexually dimorphic scale mechanoreceptors and tactile courtship in a sea snake Emydocephalus annulatus (Elapidae: Hydrophiinae)

Publisher: Oxford University Press (OUP)

Date: 07-06-2021

DOI: 10.1093/BIOLINNEAN/BLAB069

Abstract: Evolutionary transitions from terrestrial to aquatic habitats involve major selective shifts in animal signalling systems. Entirely marine snakes face two challenges during underwater social interactions: (1) finding mates when pheromones are diffused by water currents and, once a mate is located, (2) maintaining contact and co-ordinating mating when tactile cues are diminished by buoyancy force. We explore the potential tactile roles of scale protuberances in the mating of turtle-headed sea snakes [Emydocephalus annulatus (Hydrophiinae)] by investigating sexual dimorphism in museum specimens (N = 59). In addition to the previously noted rostral spine on the snout, we found that mature males have enlarged structures located on the chin (genial knobs) and near the cloaca (anal knobs). Ultrastructural data indicates that the rostral spine is comprised of thickened epidermal and dermal layers, similar to rugosities on the body, and likely provide stimulation to the female during prodding by the male. In contrast, the genial and anal knobs have dermally derived central cells indicative of enlarged scale mechanoreceptors (i.e. sensilla). We suggest that these mechanoreceptors are critical to mating success: genial knobs may help amorous males orient to the direction of female motion whereas, and anal knobs likely give somatosensory feedback for cloacal alignment

Diversity, distribution, and natural history of the marine snakes of Sri Lanka

Publisher: Springer Science and Business Media LLC

Date: 30-03-2022

DOI: 10.1007/S12526-022-01259-3

Vertebral evolution and ontogenetic allometry: The developmental basis of extreme body shape divergence in microcephalic sea snakes

Publisher: Wiley

Date: 21-02-2019

DOI: 10.1111/EDE.12284

Abstract: Snakes exhibit a erse array of body shapes despite their characteristically simplified morphology. The most extreme shape changes along the precloacal axis are seen in fully aquatic sea snakes (Hydrophiinae): "microcephalic" sea snakes have tiny heads and dramatically reduced forebody girths that can be less than a third of the hindbody girth. This morphology has evolved repeatedly in sea snakes that specialize in hunting eels in burrows, but its developmental basis has not previously been examined. Here, we infer the developmental mechanisms underlying body shape changes in sea snakes by examining evolutionary patterns of changes in vertebral number and postnatal ontogenetic growth. Our results show that microcephalic species develop their characteristic shape via changes in both the embryonic and postnatal stages. Ontogenetic changes cause the hindbodies of microcephalic species to reach greater sizes relative to their forebodies in adulthood, suggesting heterochronic shifts that may be linked to homeotic effects (axial regionalization). However, microcephalic species also have greater numbers of vertebrae, especially in their forebodies, indicating that somitogenetic effects also contribute to evolutionary changes in body shape. Our findings highlight sea snakes as an excellent system for studying the development of segment number and regional identity in the snake precloacal axial skeleton.

Venom down under: Dynamic evolution of Australian elapid snake toxins

Publisher: MDPI AG

Date: 18-12-2013

DOI: 10.3390/TOXINS5122621

Macroevolution in axial morphospace: innovations accompanying the transition to marine environments in elapid snakes

Publisher: The Royal Society

Date: 12-2022

DOI: 10.1098/RSOS.221087

Abstract: Sea snakes in the Hydrophis-Microcephalophis clade (Elapidae) show exceptional body shape variation along a continuum from similar forebody and hindbody girths, to dramatically reduced girths of the forebody relative to hindbody. The latter is associated with specializations on burrowing prey. This variation underpins high sympatric ersity and species richness and is not shared by other marine (or terrestrial) snakes. Here, we examined a hypothesis that macroevolutionary changes in axial development contribute to the propensity, at clade level, for body shape change. We quantified variation in the number and size of vertebrae in two body regions (pre- and post-apex of the heart) for approximately 94 terrestrial and marine elapids. We found Hydrophis-Microcephalophis exhibit increased rates of vertebral evolution in the pre- versus post-apex regions compared to all other Australasian elapids. Unlike other marine and terrestrial elapids, axial elongation in Hydrophis-Microcephalophis occurs via the preferential addition of vertebrae pre-heart apex, which is the region that undergoes concomitant shifts in vertebral number and size during transitions along the relative fore- to hindbody girth axis. We suggest that this macroevolutionary developmental change has potentially acted as a key innovation in Hydrophis-Microcephalophis by facilitating novel (especially burrowing) prey specializations that are not shared with other marine snakes.

Phototactic tails: Evolution and molecular basis of a novel sensory trait in sea snakes

Publisher: Wiley

Date: 15-02-2019

DOI: 10.1111/MEC.15022

Abstract: Dermal phototaxis has been reported in a few aquatic vertebrate lineages spanning fish, hibians and reptiles. These taxa respond to light on the skin of their elongate hind-bodies and tails by withdrawing under cover to avoid detection by predators. Here, we investigated tail phototaxis in sea snakes (Hydrophiinae), the only reptiles reported to exhibit this sensory behaviour. We conducted behavioural tests in 17 wild-caught sea snakes of eight species by illuminating the dorsal surface of the tail and midbody skin using cold white, violet, blue, green and red light. Our results confirmed phototactic tail withdrawal in the previously studied Aipysurus laevis, revealed this trait for the first time in A. duboisii and A. tenuis, and suggested that tail photoreceptors have peak spectral sensitivities between blue and green light (457-514 nm). Based on these results, and an absence of photoresponses in five Aipysurus and Hydrophis species, we tentatively infer that tail phototaxis evolved in the ancestor of a clade of six Aipysurus species (comprising 10% of all sea snakes). Quantifying tail damage, we found that the probability of sustaining tail injuries was not influenced by tail phototactic ability in snakes. Gene profiling showed that transcriptomes of both tail skin and body skin lacked visual opsins but contained melanopsin (opn4x) in addition to key genes of the retinal regeneration and phototransduction cascades. This work suggests that a nonvisual photoreceptor (e.g., Gq rhabdomeric) signalling pathway underlies tail phototaxis, and provides candidate gene targets for future studies of this unusual sensory innovation in reptiles.

Demographic analyses of marine and terrestrial snakes (Elapidae) using whole genome sequences

Publisher: Wiley

Date: 23-12-2020

DOI: 10.1111/MEC.15726

Horizontal transfer and subsequent explosive expansion of a DNA transposon in sea kraits ( Laticauda )

Publisher: The Royal Society

Date: 09-2021

DOI: 10.1098/RSBL.2021.0342

Abstract: Transposable elements (TEs) are self-replicating genetic sequences and are often described as important ‘drivers of evolution’. This driving force is because TEs promote genomic novelty by enabling rearrangement, and through exaptation as coding and regulatory elements. However, most TE insertions potentially lead to neutral or harmful outcomes, therefore host genomes have evolved machinery to suppress TE expansion. Through horizontal transposon transfer (HTT) TEs can colonize new genomes, and since new hosts may not be able to regulate subsequent replication, these TEs may proliferate rapidly. Here, we describe HTT of the Harbinger-Snek DNA transposon into sea kraits ( Laticauda ), and its subsequent explosive expansion within Laticauda genomes. This HTT occurred following the ergence of Laticauda from terrestrial Australian elapids approximately 15–25 Mya. This has resulted in numerous insertions into introns and regulatory regions, with some insertions into exons which appear to have altered UTRs or added sequence to coding exons. Harbinger-Snek has rapidly expanded to make up 8–12% of Laticauda spp. genomes this is the fastest known expansion of TEs in amniotes following HTT. Genomic changes caused by this rapid expansion may have contributed to adaptation to the hibious-marine habitat.

New environment, new invaders - repeated horizontal transfer of LINEs to sea snakes

Publisher: Cold Spring Harbor Laboratory

Date: 28-02-2020

DOI: 10.1101/2020.02.27.968685

Abstract: While numerous studies have found horizontal transposon transfer (HTT) to be widespread across metazoans, few have focused on HTT in marine ecosystems. To investigate potential recent HTTs into marine species we searched for novel repetitive elements in sea snakes, a group of elapids which transitioned to a marine habitat at most 18 Mya. Our analysis uncovered repeated HTTs into sea snakes following their marine transition. Such major shifts in habitat should require significant genomic changes.The seven subfamilies of horizontally transferred LINE retrotransposons we identified in the olive sea snake ( Aipysurus laevis ) are transcribed, and hence are likely still active and expanding across the genome. A search of 600 metazoan genomes found all seven were absent from other amniotes, including terrestrial elapids, with the most similar transposons present in fish and marine invertebrates. The one exception was a similar transposon found in sea kraits, a lineage of hibious elapids which independently transitioned to a marine environment following their ergence from terrestrial species 25 Mya. Our finding of repeated horizontal transfer events into separate lineages of marine snakes greatly expands past findings of frequent horizontal transfer in the marine environment, suggesting it is ideal for the transfer of transposons.Transposons are drivers of evolution as sources of genomic sequence and hence genomic novelty. This provides evidence of the environment influencing evolution of metazoans not only through specific selection pressures, but also by contributing novel genomic material.

First records of sea snakes (Elapidae: Hydrophiinae) diving to the mesopelagic zone (>200 m)

Publisher: Wiley

Date: 18-03-2019

DOI: 10.1111/AEC.12717

Patterns of intracolumnar size variation inform the heterochronic mechanisms underlying extreme body shape divergence in microcephalic sea snakes

Publisher: Wiley

Date: 15-11-2019

DOI: 10.1111/EDE.12328

Abstract: Sea snakes (Hydrophiinae) that specialize on burrowing eel prey have repeatedly evolved tiny heads and reduced forebody relative to hindbody girths. Previous research has found that these "microcephalic" forms have higher counts of precaudal vertebrae, and postnatal ontogenetic changes cause their hindbodies to reach greater girths relative to their forebodies. We examine variation in vertebral size along the precaudal axis of neonates and adults of three species. In the nonmicrocephalic Hydrophis curtus, these intracolumnar patterns take the form of symmetrical curved profiles, with longer vertebrae in the midbody (50% of body length) relative to distal regions. In contrast, intracolumnar profiles in the microcephalic H. macdowelli and H. obscurus are strongly asymmetrical curves (negative skewness) due to the presence of numerous, smaller-sized vertebrate in the forebody (anterior to the heart). Neonate and adult H. macdowelli and H. obscurus specimens all exhibit this pattern, implying an onset of fore- versus hindbody decoupling in the embryo stage. Based on this, we suggest plausible developmental mechanisms involving the presence and positioning of Hox boundaries and heterochronic changes in segmentation. Tests of our hypotheses would give new insights into the drivers of rapid convergent shifts in evolution, but will ultimately require studies of gene expression in the embryos of relevant taxa.

Horizontal transfer and subsequent explosive expansion of a DNA transposon in sea kraits (Laticauda)

Publisher: Cold Spring Harbor Laboratory

Date: 14-06-2021

DOI: 10.1101/2021.06.13.448261

Abstract: Transposable elements (TEs) are self replicating genetic sequences and are often described as important “drivers of evolution”. This driving force is because TEs promote genomic novelty by enabling rearrangement, and through exaptation as coding and regulatory elements. However, most TE insertions will be neutral or harmful, therefore host genomes have evolved machinery to supress TE expansion. Through horizontal transposon transfer (HTT) TEs can colonise new genomes, and since new hosts may not be able to shut them down, these TEs may proliferate rapidly. Here we describe HTT of the Harbinger-Snek DNA transposon into sea kraits ( Laticauda ), and its subsequent explosive expansion within Laticauda genomes. This HTT occurred following the ergence of Laticauda from terrestrial Australian elapids ~15-25 Mya. This has resulted in numerous insertions into introns and regulatory regions, with some insertions into exons which appear to have altered UTRs or added sequence to coding exons. Harbinger-Snek has rapidly expanded to make up 8-12% of Laticauda spp. genomes this is the fastest known expansion of TEs in amniotes following HTT. Genomic changes caused by this rapid expansion may have contributed to adaptation to the hibious-marine habitat.

Ultrastructural evidence of a mechanosensory function of scale organs (sensilla) in sea snakes (Hydrophiinae)

Publisher: The Royal Society

Date: 04-2019

DOI: 10.1098/RSOS.182022

Abstract: The evolution of epidermal scales was a major innovation in lepidosaurs, providing a barrier to dehydration and physical stress, while functioning as a sensitive interface for detecting mechanical stimuli in the environment. In snakes, mechanoreception involves tiny scale organs (sensilla) that are concentrated on the surface of the head. The fully marine sea snakes (Hydrophiinae) are closely related to terrestrial hydrophiine snakes but have substantially more protruding (dome-shaped) scale organs that often cover a larger portion of the scale surface. Various ergent selection pressures in the marine environment could account for this morphological variation relating to detection of mechanical stimuli from direct contact with stimuli and/or indirect contact via water motion (i.e. ‘hydrodynamic reception’), or co-option for alternate sensory or non-sensory functions. We addressed these hypotheses using immunohistochemistry, and light and electron microscopy, to describe the cells and nerve connections underlying scale organs in two sea snakes, Aipysurus laevis and Hydrophis stokesii . Our results show ultrastructural features in the cephalic scale organs of both marine species that closely resemble the mechanosensitive Meissner-like corpuscles that underlie terrestrial snake scale organs. We conclude that the scale organs of marine hydrophiines have retained a mechanosensory function, but future studies are needed to examine whether they are sensitive to hydrodynamic stimuli.

Evidence for a Müllerian mimetic radiation in Asian pitvipers

Publisher: The Royal Society

Date: 08-02-2006

DOI: 10.1098/RSPB.2005.3418

Abstract: Müllerian mimicry, in which toxic species gain mutual protection from shared warning signals, is poorly understood in vertebrates, reflecting a paucity of ex les. Indirect evidence for mimicry is found if monophyletic species or clades show parallel geographic variation in warning patterns. Here, we evaluate a hypothesis of Müllerian mimicry for the pitvipers in Southeast Asia using a phylogeny derived from DNA sequences from four combined mitochondrial regions. Mantel matrix correlation tests show that conspicuous red colour pattern elements are significantly associated with sympatric and parapatric populations in four genera. To our knowledge, this represents the first evidence of a Müllerian mimetic radiation in vipers. The putative mimetic patterns are rarely found in females. This appears paradoxical in light of the Müllerian prediction of monomorphism, but may be explained by ergent selection pressures on the sexes, which have different behaviours. We suggest that biased predation on active males causes selection for protective warning coloration, whereas crypsis is favoured in relatively sedentary females.

Heterochronic Shifts Mediate Ecomorphological Convergence in Skull Shape of Microcephalic Sea Snakes

Publisher: Oxford University Press (OUP)

Date: 07-05-2019

DOI: 10.1093/ICB/ICZ033

Abstract: Morphological variation among the viviparous sea snakes (Hydrophiinae), a clade of fully aquatic elapid snakes, includes an extreme “microcephalic” ecomorph that has a very small head atop a narrow forebody, while the hind body is much thicker (up to three times the forebody girth). Previous research has demonstrated that this morphology has evolved at least nine times as a consequence of dietary specialization on burrowing eels, and has also examined morphological changes to the vertebral column underlying this body shape. The question addressed in this study is what happens to the skull during this extreme evolutionary change? Here we use X-ray micro-computed tomography and geometric morphometric methods to characterize cranial shape variation in 30 species of sea snakes. We investigate ontogenetic and evolutionary patterns of cranial shape ersity to understand whether cranial shape is predicted by dietary specialization, and examine whether cranial shape of microcephalic species may be a result of heterochronic processes. We show that the diminutive cranial size of microcephalic species has a convergent shape that is correlated with trophic specialization to burrowing prey. Furthermore, their cranial shape is predictable for their size and very similar to that of juvenile in iduals of closely related but non-microcephalic sea snakes. Our findings suggest that heterochronic changes (resulting in pedomorphosis) have driven cranial shape convergence in response to dietary specializations in sea snakes.

Underwater hearing in sea snakes (Hydrophiinae): first evidence of auditory evoked potential thresholds

Publisher: The Company of Biologists

Date: 15-07-2019

DOI: 10.1242/JEB.198184

Abstract: The viviparous sea snakes (Hydrophiinae) are a secondarily aquatic radiation of more than 60 species that possess many phenotypic adaptations to marine life. However, virtually nothing is known of the role and sensitivity of hearing in sea snakes. This study investigated the hearing sensitivity of the fully marine sea snake Hydrophis stokesii by measuring auditory evoked potential (AEP) audiograms for two in iduals. AEPs were recorded from 40 Hz (the lowest frequency tested) up to 600 Hz, with a peak in sensitivity identified at 60 Hz (163.5 dB re. 1 µPa or 123 dB re. 1 µm s−2). Our data suggest that sea snakes are sensitive to low-frequency sounds but have relatively low sensitivity compared with bony fishes and marine turtles. Additional studies are required to understand the role of sound in sea snake life history and further assess these species' vulnerability to anthropogenic noise.

Trophic specialization drives morphological evolution in sea snakes

Publisher: The Royal Society

Date: 03-2018

DOI: 10.1098/RSOS.172141

Abstract: Viviparous sea snakes are the most rapidly speciating reptiles known, yet the ecological factors underlying this radiation are poorly understood. Here, we reconstructed dated trees for 75% of sea snake species and quantified body shape (forebody relative to hindbody girth), maximum body length and trophic ersity to examine how dietary specialization has influenced morphological ersification in this rapid radiation. We show that sea snake body shape and size are strongly correlated with the proportion of burrowing prey in the diet. Specialist predators of burrowing eels have convergently evolved a ‘microcephalic’ morphotype with dramatically reduced forebody relative to hindbody girth and intermediate body length. By comparison, snakes that predominantly feed on burrowing gobies are generally short-bodied and small-headed, but there is no evidence of convergent evolution. The eel specialists also exhibit faster rates of size and shape evolution compared to all other sea snakes, including those that feed on gobies. Our results suggest that trophic specialization to particular burrowing prey (eels) has invoked strong selective pressures that manifest as predictable and rapid morphological changes. Further studies are needed to examine the genetic and developmental mechanisms underlying these dramatic morphological changes and assess their role in sea snake speciation.

Horizontal transposon transfer and its implications for the ancestral ecology of hydrophiine snakes

Publisher: Cold Spring Harbor Laboratory

Date: 23-06-2021

DOI: 10.1101/2021.06.22.449521

Abstract: Transposable elements (TEs), also known as jumping genes, are sequences able to move or copy themselves within a genome. As TEs move throughout genomes they often act as a source of genetic novelty, hence understanding TE evolution within lineages may help in understanding environmental adaptation. Studies into the TE content of lineages of mammals such as bats have uncovered horizontal transposon transfer (HTT) into these lineages, with squamates often also containing the same TEs. Despite the repeated finding of HTT into squamates, little comparative research has examined the evolution of TEs within squamates. Here we examine a erse family of Australo-Melanesian snakes (Hydrophiinae) to examine if the previously identified, order-wide pattern of variable TE content and activity holds true on a smaller scale. Hydrophiinae erged from Asian elapids ∼30 Mya and have since rapidly ersified into six hibious, ∼60 marine and ∼100 terrestrial species which fill a broad range of ecological niches. We find TE ersity and expansion differs between hydrophiines and their Asian relatives and identify multiple HTTs into Hydrophiinae, including three likely transferred into the ancestral hydrophiine from fish. These HTT events provide the first tangible evidence that Hydrophiinae reached Australia from Asia via a marine route.

Diversification rates and phenotypic evolution in venomous snakes (Elapidae)

Publisher: The Royal Society

Date: 2016

DOI: 10.1098/RSOS.150277

Abstract: The relationship between rates of ersification and of body size change (a common proxy for phenotypic evolution) was investigated across Elapidae, the largest radiation of highly venomous snakes. Time-calibrated phylogenetic trees for 175 species of elapids (more than 50% of known taxa) were constructed using seven mitochondrial and nuclear genes. Analyses using these trees revealed no evidence for a link between speciation rates and changes in body size. Two clades ( Hydrophis , Micrurus ) show anomalously high rates of ersification within Elapidae, yet exhibit rates of body size evolution almost identical to the general elapid ‘background’ rate. Although correlations between speciation rates and rates of body size change exist in certain groups (e.g. ray-finned fishes, passerine birds), the two processes appear to be uncoupled in elapid snakes. There is also no detectable shift in ersification dynamics associated with the colonization of Australasia, which is surprising given that elapids appear to be the first clade of venomous snakes to reach the continent.

Uncoupling ecological innovation and speciation in sea snakes (Elapidae, Hydrophiinae, Hydrophiini)

Publisher: Wiley

Date: 12-10-2010

DOI: 10.1111/J.1420-9101.2010.02131.X

Abstract: The viviparous sea snakes (Hydrophiini) are by far the most successful living marine reptiles, with ∼ 60 species that comprise a prominent component of shallow-water marine ecosystems throughout the Indo-West Pacific. Phylogenetically nested within the ∼ 100 species of terrestrial Australo-Melanesian elapids (Hydrophiinae), molecular timescales suggest that the Hydrophiini are also very young, perhaps only ∼ 8-13 Myr old. Here, we use likelihood-based analyses of combined phylogenetic and taxonomic data for Hydrophiinae to show that the initial invasion of marine habitats was not accompanied by elevated ersification rates. Rather, a dramatic three to six-fold increase in ersification rates occurred at least 3-5 Myr after this transition, in a single nested clade: the Hydrophis group accounts for ∼ 80% of species richness in Hydrophiini and ∼ 35% of species richness in (terrestrial and marine) Hydrophiinae. Furthermore, other co-distributed lineages of viviparous sea snakes (and marine Laticauda, Acrochordus and homalopsid snakes) are not especially species rich. Invasion of the oceans has not (by itself) accelerated ersification in Hydrophiini novelties characterizing the Hydrophis group alone must have contributed to its evolutionary and ecological success.

Novel vascular plexus in the head of a sea snake (Elapidae, Hydrophiinae) revealed by high-resolution computed tomography and histology

Publisher: The Royal Society

Date: 04-09-2019

DOI: 10.1098/RSOS.191099

Abstract: Novel phenotypes are often linked to major ecological transitions during evolution. Here, we describe for the first time an unusual network of large blood vessels in the head of the sea snake Hydrophis cyanocinctus . MicroCT imaging and histology reveal an intricate modified cephalic vascular network (MCVN) that underlies a broad area of skin between the snout and the roof of the head. It is mostly composed of large veins and sinuses and converges posterodorsally into a large vein (sometimes paired) that penetrates the skull through the parietal bone. Endocranially, this blood vessel leads into the dorsal cerebral sinus, and from there, a pair of large veins depart ventrally to enter the brain. We compare the condition observed in H. cyanocinctus with that of other elapids and discuss the possible functions of this unusual vascular network. Sea snakes have low oxygen partial pressure in their arterial blood that facilitates cutaneous respiration, potentially limiting the availability of oxygen to the brain. We conclude that this novel vascular structure draining directly to the brain is a further elaboration of the sea snakes' cutaneous respiratory anatomy, the most likely function of which is to provide the brain with an additional supply of oxygen.

Functional Duplication of the Short-Wavelength-Sensitive Opsin in Sea Snakes: Evidence for Reexpanded Color Sensitivity Following Ancestral Regression

Publisher: Oxford University Press (OUP)

Date: 07-2023

DOI: 10.1093/GBE/EVAD107

Abstract: Color vision is mediated by ancient and spectrally distinct cone opsins. Yet, while there have been multiple losses of opsin genes during the evolution of tetrapods, evidence for opsin gains via functional duplication is extremely scarce. Previous studies have shown that some secondarily marine elapid snakes have acquired expanded “UV–blue” sensitivity via changes at key spectral tuning amino acid sites of the Short-Wavelength Opsin 1 (SWS1) gene. Here, we use elapid reference genomes to show that the molecular origin of this adaptation involved repeated, proximal duplications of the SWS1 gene in the fully marine Hydrophis cyanocinctus. This species possesses four intact SWS1 genes two of these genes have the ancestral UV sensitivity, and two have a derived sensitivity to the longer wavelengths that dominate marine habitats. We suggest that this remarkable expansion of the opsin repertoire of sea snakes functionally compensates for the ancestral losses of two middle-wavelength opsins in the earliest (dim-light adapted) snakes. This provides a striking contrast to the evolution of opsins during ecological transitions in mammals. Like snakes, early mammals lost two cone photopigments however, lineages such as bats and cetaceans underwent further opsin losses during their adaptation to dim-light environments.

Multilocus phylogeny and recent rapid radiation of the viviparous sea snakes (Elapidae: Hydrophiinae)

Publisher: Elsevier BV

Date: 03-2013

DOI: 10.1016/J.YMPEV.2012.09.021

Abstract: The viviparous sea snakes (Hydrophiinae: Hydrophiini) comprise a young but morphologically and ecologically erse clade distributed throughout the Indo-Pacific. Despite presenting a very promising model for marine ersification studies, many relationships among the 62 species and 16 genera in Hydrophiini remain unresolved. Here, we extend previous taxonomic and genomic s ling for Hydrophiini using three mitochondrial fragments and five nuclear loci for multiple in iduals of 39 species in 15 genera. Our results highlight many of the impediments to inferring phylogenies in recent rapid radiations, including low variation at all five nuclear markers, and conflicting relationships supported by mitochondrial and nuclear trees. However, concatenated Bayesian and likelihood analyses, and a multilocus coalescent tree, recovered concordant support for primary clades and several previously unresolved inter-specific groupings. The Aipysurus group is monophyletic, with egg-eating specialists forming separate, early- erging lineages. All three monotypic semi-aquatic genera (Ephalophis, Parahydrophis and Hydrelaps) are robustly placed as early erging lineages along the branch leading to the Hydrophis group, with Ephalophis recovered as sister to Parahydrophis. The molecular phylogeny implies extensive evolutionary convergence in feeding adaptations within the Hydrophis group, especially the repeated evolution of small-headed (microcephalic) forms. Microcephalophis (Hydrophis) gracilis is robustly recovered as a relatively distant sister lineage to all other s led Hydrophis group species, here termed the 'core Hydrophis group'. Within the 'core Hydrophis group', Hydrophis is recovered as broadly paraphyletic, with several other genera nested within it (Pelamis, Enhydrina, Astrotia, Thalassophina, Acalyptophis, Kerilia, Lapemis, Disteira). Instead of erecting multiple new genera, we recommend dismantling the latter (mostly monotypic) genera and recognising a single genus, Hydrophis Latreille 1802, for the core Hydrophis group. Estimated ergence times suggest that all Hydrophiini last shared a common ancestor ∼6million years ago, but that the majority of extant lineages ersified over the last ∼3.5million years. The core Hydrophis group is a young and rapidly speciating clade, with 26 s led species and 9 genera and dated at only ∼1.5-3million years old.

Molecular evidence for a rapid late-Miocene radiation of Australasian venomous snakes (Elapidae, Colubroidea)

Publisher: Elsevier BV

Date: 03-2008

DOI: 10.1016/J.YMPEV.2007.11.013

Molecular phylogeny and divergence dates for Australasian elapids and sea snakes (hydrophiinae): evidence from seven genes for rapid evolutionary radiations

Publisher: Wiley

Date: 31-03-2008

DOI: 10.1111/J.1420-9101.2008.01525.X

Abstract: One of the most prolific radiations of venomous snakes, the Australo-Melanesian Hydrophiinae includes approximately 100 species of Australasian terrestrial elapids plus all approximately 60 species of viviparous sea snakes. Here, we estimate hydrophiine relationships based on a large data set comprising 5800 bp drawn from seven genes (mitochondrial: ND4, cytb, 12S, 16S nuclear: rag1, cmos, myh). These data were analysed using parsimony, likelihood and Bayesian methods to better resolve hydrophiine phylogeny and provide a timescale for the terrestrial and marine radiations. Among oviparous forms, Cacophis, Furina and Demansia are basal to other Australian elapids (core oxyuranines). The Melanesian Toxicocalamus and Aspidomorphus group with Demansia, indicating multiple dispersal events between New Guinea and Australia. Oxyuranus and Pseudonaja form a robust clade. The small burrowing taxa form two separate clades, one consisting of Vermicella and Neelaps calanotus, and the other including Simoselaps, Brachyurophis and Neelaps bimaculatus. The viviparous terrestrial elapids form three separate groups: Acanthophis, the Rhinoplocephalus group and the Notechis-Hemiaspis group. True sea snakes (Hydrophiini) are robustly united with the Notechis-Hemiaspis group. Many of the retrieved groupings are consistent with previous molecular and morphological analyses, but the polyphyly of the viviparous and burrowing groups, and of Neelaps, are novel results. Bayesian relaxed clock analyses indicate very recent ergences: the approximately 160 species of the core Australian radiation (including sea snakes) arose within the last 10 Myr, with most inter-generic splits dating to between 10 and 6 Ma. The Hydrophis sea snake lineage is an exceptionally rapid radiation, with > 40 species evolving within the last 5 Myr.

First evidence of hemiclitores in snakes

Publisher: The Royal Society

Date: 14-12-2022

DOI: 10.1098/RSPB.2022.1702

Abstract: Female genitalia are conspicuously overlooked in comparison to their male counterparts, limiting our understanding of sexual reproduction across vertebrate lineages. This study is the first complete description of the clitoris (hemiclitores) in female snakes. We describe morphological variation in size and shape ( n = 9 species, 4 families) that is potentially comparable to the male intromittent organs in squamate reptiles (hemipenes). Dissection, diffusible iodine contrast-enhanced micro-CT and histology revealed that, unlike lizard hemiclitores, the snake hemiclitores are non-eversible structures. The two in idual hemiclitores are separated medially by connective tissue, forming a triangular structure that extends posteriorly. Histology of the hemiclitores in Australian death adders ( Acanthophis antarcticus ) showed erectile tissue and strands/bundles of nerves, but no spines (as is found in male hemipenes). These histological features suggest the snake hemiclitores have functional significance in mating and definitively show that the hemiclitores are not underdeveloped hemipenes or scent glands, which have been erroneously indicated in other studies. Our discovery supports that hemiclitores have been retained across squamates and provides preliminary evidence of differences in this structure among snake species, which can be used to further understand systematics, reproductive evolution and ecology across squamate reptiles.

Rates of population differentiation and speciation are decoupled in sea snakes

Publisher: The Royal Society

Date: 10-2018

DOI: 10.1098/RSBL.2018.0563

Abstract: Comparative phylogeography can inform many macroevolutionary questions, such as whether species ersification is limited by rates of geographical population differentiation. We examined the link between population genetic structure and species ersification in the fully aquatic sea snakes (Hydrophiinae) by comparing mitochondrial phylogeography across northern Australia in 16 species from two closely related clades that show contrasting ersification dynamics. Contrary to expectations from theory and several empirical studies, our results show that, at the geographical scale studied here, rates of population differentiation and speciation are not positively linked in sea snakes. The eight species s led from the rapidly speciating Hydrophis clade have weak population differentiation that lacks geographical structure. By contrast, all eight s led Aipysurus–Emydocephalus species show clear geographical patterns and many deep intraspecific splits, but have threefold slower speciation rates. Alternative factors, such as ecological specialization, species duration and geographical range size, may underlie rapid speciation in sea snakes.

University Of Adelaide

Location: Australia

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