Heterochronic shifts mediate ecomorphological convergence in skull shape of microcephalic sea snakes

Abstract

Among the viviparous sea snakes (Hydrophiinae), a clade of fully aquatic elapid snakes, exists an extreme ‘microcephalic’ ecomorph that has a very small head atop a narrow forebody, while the hind body is much thicker and terminates in a paddle-like tail. Previous research has demonstrated that this morphology has evolved at least nine times as a consequence of dietary specialisation on burrowing eels, and 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 characterise skull shape variation in 30 species of sea snakes. We investigate ontogenetic and evolutionary patterns of skull shape diversity to understand the extent that skull shape is predicted by dietary specialisation and examine whether skull shape of microcephalic species may be a result of heterochronic processes. We show that the diminutive skull size of microcephalic species has a convergent shape that is correlated with trophic specialisation to burrowing prey. Furthermore, their skull shape is predictable for their size and very similar to juvenile individuals of closely related but non-microcephalic sea snakes. This ecomorph thus appears to have evolved by heterochronic processes, with the skull resembling a paedomorphic form. Our findings suggest that heterochronic changes (resulting in paedomorphosis) have driven skull shape convergence in response to dietary specialisations in sea snakes, leading to repeated and relatively rapid changes in growth and its timing resulting in dramatically altered morphologies.