The study of convergently acquired adaptations allows fundamental insight into life’s evolutionary history. Within lepidosaur reptiles—i.e. lizards, tuatara, and snakes—a fully fossorial (‘burrowing’) lifestyle has independently evolved in most major clades. However, despite their consistent use of the skull as a digging tool, cranial modifications common to all these lineages are yet to be found. In particular, bone microanatomy, although highly diagnostic for lifestyle, remains unexplored in the lepidosaur cranium. This constitutes a key gap in our understanding of their complexly interwoven ecology, morphology, and evolution. In order to bridge this gap, we reconstructed the acquisition of a fossorial lifestyle in 2813 lepidosaurs and assessed the skull roof compactness from microCT cross-sections in a representative subset (n = 99). We tested this and five macroscopic morphological traits for their convergent evolution. We found that fossoriality evolved independently in 54 lepidosaur lineages. Furthermore, a highly compact skull roof, small skull diameter, elongate cranium, and low length ratio of frontal and parietal were repeatedly acquired in concert with a fossorial lifestyle. We report a novel case of convergence that concerns lepidosaur diversity as a whole. Our findings further indicate an early evolution of fossorial modifications in the amphisbaenian ‘worm-lizards’ and support a fossorial origin for snakes. Nonetheless, our results suggest distinct evolutionary pathways between fossorial lizards and snakes through different contingencies. We thus provide novel insights into the evolutionary mechanisms and constraints underlying amniote diversity and a powerful tool for the reconstruction of extinct reptile ecology.

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First evidence of convergent lifestyle signal in reptile skull roof microanatomy

Rensch's rule relates to a pattern whereby sexual size dimorphism (SSD) is more female-biased in small-sized species and more male-biased in large-sized ones. We collected literature and museum data on the body size of males and females belonging to 4,032 lizard species, as well as data on their reproductive modes and clutch sizes. We used phylogenetic comparative analyses, and general linear mixed models, to test Rensch's rule and examined how reproductive mode and clutch size affect sexual size dimorphism. Sexual size dimorphism was independent of clutch size in lizard species with variable clutch sizes and in oviparous lizards. Large litters were associated with female-biased sexual dimorphism in viviparous and in scincomorph lizards. Inference regarding Rensch's rule depended on the analytical method used to identify it. The widely used, but less conservative, reduced major axis regression usually support Rensch's rule while ordinary least squares regressions mostly show isometric relationships. The rule tended to apply more to oviparous than viviparous lizards. We infer that Rensch's rule is, at best, a weak pattern in lizards. This is especially true in viviparous lineages, where females reproduce infrequently, therefore evolve large sizes to maximise fecundity, resulting in female-biased dimorphism. This article is protected by copyright. All rights reserved.

Sexual size dimorphism in lizards: Rensch's rule, reproductive mode, clutch size, and line fitting method effects.

Lungless salamanders (Family Plethodontidae) form a highly speciose group that has undergone spectacular adaptive radiation to colonize a multitude of habitats. Substantial morphological variation in the otic region coupled with great ecological diversity within this clade make plethodontids an excellent model for exploring the ecomorphology of the amphibian ear. We examined the influence of habitat, development, and vision on inner ear morphology in 52 plethodontid species. We collected traditional and 3D geometric morphometric measurements to characterize variation in size and shape of the otic endocast and peripheral structures of the salamander ear. Phylogenetic comparative analyses demonstrate structural convergence in the inner ear across ecologically similar species. Species that dwell in spatially complex microhabitats exhibit robust, highly curved semicircular canals suggesting enhanced vestibular sense, whereas species with reduced visual systems demonstrate reduced canal curvature indicative of relaxed selection on the vestibulo-ocular reflex. Cave specialists show parallel enlargement of auditory-associated structures. The morphological correlates of ecology among diverse species reveal underlying evidence of habitat specialization in the inner ear and suggest that there exists physiological variation in the function of the salamander ear even in the apparent absence of selective pressures on the auditory system to support acoustic behavior.

Bony labyrinth morphometry reveals hidden diversity in lungless salamanders (Family Plethodontidae): Structural correlates of ecology, development, and vision in the inner ear.

Burrowing is a common behavior in vertebrates. An underground life-style offers many advantages but also poses important challenges including the high energetic cost of burrowing. Scolecophidians are a group of morphologically derived subterranean snakes that show great diversity in form and function. Although it has been suggested that leptotyphlopids and anomalepidids mostly use existing underground passageways, typhlopids are thought to create their own burrows. However, the mechanisms used to create burrows and the associated forces that animals may be able to generate remain unknown. Here, we provide the first data on push forces in scolecophidians and compare them with those in some burrowing alethinophidian snakes. Our results show that typhlopids are capable of generating higher forces for a given size than other snakes. The observed differences are not due to variation in body diameter or length, suggesting fundamental differences in the mechanics of burrowing or the way in which axial muscles are used. Qualitative observations of skull and vertebral shape suggest that the higher forces exerted by typhlopids may have impacted the evolution of their anatomy. Our results provide the basis for future studies exploring the diversity of form and function in this fascinating group of animals. Quantitative comparisons of the cranial and vertebral shape in addition to collecting functional and ecological data on a wider array of species would be particularly important to test the patterns described here.

Burrowing in blindsnakes: A preliminary analysis of burrowing forces and consequences for the evolution of morphology

Caecilians are elongate, limbless and annulated amphibians that, with the exception of one aquatic family, all have an at least partly fossorial lifestyle. It has been suggested that caecilian evolution resulted in sturdy and compact skulls with fused bones and tight sutures, as an adaptation to their head-first burrowing habits. However, although their cranial osteology is well described, relationships between form and function remain poorly understood. In the present study, we explored the relationship between cranial shape and in vivo burrowing forces. Using micro-computed tomography (µCT) data, we performed 3D geometric morphometrics to explore whether cranial and mandibular shapes reflected patterns that might be associated with maximal push forces. The results highlight important differences in maximal push forces, with the aquatic Typhlonectes producing a lower force for a given size compared with other species. Despite substantial differences in head morphology across species, no relationship between overall skull shape and push force could be detected. Although a strong phylogenetic signal may partly obscure the results, our conclusions confirm previous studies using biomechanical models and suggest that differences in the degree of fossoriality do not appear to be driving the evolution of head shape.

Under pressure: the relationship between cranial shape and burrowing force in caecilians (Gymnophiona).

1UMR 7179 C.N.R.S/M.N.H.N., Département Adaptations du Vivant, Bâtiment d’Anatomie Comparée, 55 rue Buffon, 75005, Paris, France 2Institut de Systématique, Evolution, Biodiversité, (UMR 7205 Muséum national d’Histoire naturelle, CNRS UPMC EPHE, Sorbonne Universités), CP30, 25 rue Cuvier 75005, Paris, France 3Centre for Invasion Biology, Department of Botany & Zoology, Stellenbosch University, Private Bag X1, 7602 Matieland, Stellenbosch, South Africa 4Deparment of Biology, University of Antwerp, Universiteitsplein 1, B2610 Antwerpen, Belgium 5Department of Biomedical Sciences, Ohio University, Cleveland Campus, SPS-334C, Cleveland, 45701 Ohio, USA 6Department of Biology, Evolutionary Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium

Trade-offs between burrowing and biting force in fossorial scincid lizards?

Amphibians are different from most other tetrapods because they have a biphasic life cycle, with larval forms showing a dramatically different cranial anatomy and feeding strategy compared to adults. Amphibians with their exceptional diversity in habitats, lifestyles and reproductive modes are also excellent models for studying the evolutionary divergence in feeding systems. In the present chapter, we review the literature on amphibian feeding anatomy and function published since 2000. We also present some novel unpublished data on caecilian feeding biomechanics. This review shows that over the past two decades important new insights in our understanding of amphibian feeding anatomy and function have been made possible, thanks to a better understanding of the phylogenetic relationships between taxa, analyses of development and the use of biomechanical modelling. In terms of functional analyses, important advances involve the temperature-dependent nature of tongue projection mechanisms and the plasticity exhibited by animals when switching environments (land to water) during their lifetime. Understanding the relationships between cranial and hyobranchial diversity and feeding function, and how these relationships are dependent on lifestyle, habitat use or reproductive mode are questions that remain to be answered. Given the availability of massive online databases with µCT data and robust comprehensive phylogenies, these analyses are becoming possible. Unfortunately, quantitative studies on muscular anatomy, essential to link variation in form to variation in function using modelling approaches, have lagged behind. Future studies quantifying feeding across a wide range of species will provide critical insights into the selective pressures underlying the evolution of the staggering diversity in feeding form and function of amphibians.

James C. O’Reilly

Papers

Trade-offs between burrowing and biting force in fossorial scincid lizards?

Feeding in Amphibians: Evolutionary Transformations and Phenotypic Diversity as Drivers of Feeding System Diversity

Under pressure: the relationship between cranial shape and burrowing force in caecilians (Gymnophiona).