Sexual dimorphism in size and shape of the head in the sea snake Emydocephalus annulatus (Hydrophiinae, Elapidae).

In snakes, divergence in head size between the sexes has been interpreted as an adaptation to intersexual niche divergence. By overcoming gape-limitation, a larger head enables snakes of one sex to ingest larger prey items. Under this hypothesis, we do not expect a species that consumes only tiny prey items to exhibit sex differences in relative head size, or to show empirical links between relative head size and fitness-relevant traits such as growth and fecundity. Our field studies on the sea snake Emydocephalus annulatus falsify these predictions. Although these snakes feed exclusively on fish eggs, the heads of female snakes are longer and wider than those of males at the same body length. Individuals with wider heads grew more rapidly, reproduced more often, and produced larger litters. Thus, head shape can affect fitness and can diverge between the sexes even without gape-limitation. Head size and shape may facilitate other aspects of feeding (such as the ability to scrape eggs off coral) and locomotion (hydrodynamics); and a smaller head may advantage the sex that is more mobile, and that obtains its prey in narrow crevices rather than in more exposed situations (i.e., males).

De Novo Venom-Gland Transcriptomics of Spine-Bellied Sea Snake (Hydrophis curtus) from Penang, Malaysia-Next-Generation Sequencing, Functional Annotation and Toxinological Correlation.

Envenomation resulted from sea snake bite is a highly lethal health hazard in Southeast Asia. Although commonly caused by sea snakes of Hydrophiinae, each species is evolutionarily distinct and thus, unveiling the toxin gene diversity within individual species is important. Applying next-generation sequencing, this study investigated the venom-gland transcriptome of Hydrophis curtus (spine-bellied sea snake) from Penang, West Malaysia. The transcriptome was de novo assembled, followed by gene annotation and sequence analyses. Transcripts with toxin annotation were only 96 in number but highly expressed, constituting 48.18% of total FPKM in the overall transcriptome. Of the 21 toxin families, three-finger toxins (3FTX) were the most abundantly expressed and functionally diverse, followed by phospholipases A2. Lh_FTX001 (short neurotoxin) and Lh_FTX013 (long neurotoxin) were the most dominant 3FTXs expressed, consistent with the pathophysiology of envenomation. Lh_FTX001 and Lh_FTX013 were variable in amino acid compositions and predicted epitopes, while Lh_FTX001 showed high sequence similarity with the short neurotoxin from Hydrophis schistosus, supporting cross-neutralization effect of Sea Snake Antivenom. Other toxins of low gene expression, for example, snake venom metalloproteinases and L-amino acid oxidases not commonly studied in sea snake venom were also identified, enriching the knowledgebase of sea snake toxins for future study.

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

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.

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

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 diversity 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 individuals 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.

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

Snakes exhibit a diverse 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.

Structure and function of skin in the pelagic sea snake, Hydrophis platurus.

We describe and interpret the functional morphology of skin of the Yellow-bellied sea snake, Hydrophis platurus. This is the only pelagic sea snake, and its integument differs from what is known for other species of snakes. In gross appearance, the scales of H. platurus consist of non-overlapping, polygonal knobs with flattened outer surfaces bearing presumptive filamentous sensillae. The deep recesses between scales ('hinge') entrap and wick water over the body surface, with mean retention of 5.1 g/cm of skin surface, similar to that determined previously for the roughened, spiny skin of marine file snakes, Acrochordus granulatus. This feature possibly serves to maintain the skin wet when the dorsal body protrudes above water while floating on calm oceanic slicks where they forage. In contrast with other snakes, including three species of amphibious, semi-marine sea kraits (Laticauda spp.), the outer corneous ß-protein layer consists of a syncytium that is thinner than seen in most other species. The subjacent α-layer is also thin, and lipid droplets and lamellar bodies are seen among the immature, cornifying α-cells. A characteristic mesos layer, comprising the water permeability barrier, is either absent or very thin. These features are possibly related to (1) permeability requirements for cutaneous gas exchange, (2) reduced gradient for water efflux compared with terrestrial environments, (3) less need for physical protection in water compared with terrestrial ground environments, and (4) increased frequency of ecdysis thought to be an anti-fouling mechanism. The lipogenic features of the α-layer possibly compensate for the reduced or absent mesos layer, or produce layers of cells that comprise what functionally might be termed a mesos layer, but where the organization of barrier lipids nonetheless appears less robust than what is characteristically seen in squamates.

Postmortem examination of Australian sea snakes ( Hydrophiinae): Anatomy and common pathologic conditions.

There is limited published information about disease in wild sea snakes and no standardized guideline for postmortem examination of sea snakes. Identifying causes of morbidity and mortality of marine vertebrate species has been pivotal to understanding disease factors implicated in stranding events and assisting with the formulation of conservation plans. Additionally, postmortem findings can provide valuable information on life history traits and the ecology of these reclusive species. Sick, moribund, or dead sea snakes are intermittently washed ashore along Australian and international beaches and provide an opportunity to examine a subset of the population and identify causes of population decline. We present an illustrated description of sea snake anatomy and describe a systematic approach to postmortem examination of sea snakes. We describe common pathologic conditions identified from clinical and postmortem examinations of stranded Australian sea snakes from southeast Queensland. Notable pathologic conditions include traumatic injury, inflammatory conditions, parasitic infections, and neoplasia.