Phylogenetic history influences convergence for a specialized ecology: comparative skull morphology of African burrowing skinks (Squamata; Scincidae)

Abstract

Background Skulls serve many functions and as a result, are subject to many different evolutionary pressures. In squamates, many fossorial species occupy a unique region of skull morphospace, showing convergence across families, due to modifications related to head-first burrowing. As different substrates have variable physical properties, particular skull shapes may offer selective advantages in certain substrates. Despite this, studies of variation within burrowers have been limited and are typically focused on a single origin of fossoriality. We focused on seven skink genera (Acontias, Typhlosaurus, Scelotes, Sepsina, Feylinia, Typhlacontias, and Mochlus; 39 sp.) from southern Africa, encompassing at least three independent evolutions of semi-fossoriality/fossoriality. We used microCT scans and geometric morphometrics to test how cranial and mandibular shape were influenced by phylogenetic history, size, and ecology. We also qualitatively described the skulls of four species to look at variation across phylogenetic and functional levels, and assess the degree of convergence. Results We found a strong effect of phylogenetic history on cranial and mandibular shape, with size and substrate playing secondary roles. There was a clear gradient in morphospace from less specialized to more specialized burrowers and burrowers in sand were significantly different from those in other substrates. We also created an anatomical atlas for four species with each element described in isolation. Every bone showed some variation in shape and relative scaling of features, with the skull roofing bones, septomaxilla, vomer, and palatine showing the most variation. We showed how broad-scale convergence in traits related to fossoriality can be the result of different anatomical changes. Conclusions Our study used geometric morphometrics and comparative anatomy to examine how skull morphology changes for a highly specialized and demanding lifestyle. Although there was broad convergence in both shape and qualitative traits, phylogenetic history played a large role and much of this convergence was produced by different anatomical changes, implying different developmental pathways or lineage-specific constraints. Even within a single family, adaptation for a specialized ecology does not follow a singular deterministic path.

Macroecological and biogeographical patterns of limb reduction in the world's skinks

“…Sand (and by extension, sandy soil) is known to behave like a frictional granular fluid (Attum et al, 2007; Crofts & Summers, 2011), which would select for smaller body sizes due to the low relative force needed to penetrate it (Arnold, 1995; Pough et al, 1997). Substrates rich in organic matter (‘humus’) would select for smaller body sizes as they tend to be relatively soft, not requiring much applied force to penetrate—and thus, not a large mass or size (Stepanova & Bauer, 2021). Indeed, when considering SVL in isolation, we find that species living in humus are significantly shorter than all categories except sand and sandy soil (Figure 3c).…”

“…Indeed, when considering SVL in isolation, we find that species living in humus are significantly shorter than all categories except sand and sandy soil (Figure 3c). Conversely, more compacted substrates (the ‘soil’ category) would require larger bodes to push through more resistant material, associated with head‐first burrowing strategies (Bergmann & Berry, 2021; Kazi & Hipsley, 2018; Müller et al, 2011; Stepanova & Bauer, 2021). An example of such a functional niche‐driven size differentiation is the sub‐Saharan skink subfamily Acontinae, whose larger forms are associated with more compact soils, whereas smaller ones are sand‐swimmers (Branch, 1998; Lamb et al, 2010; Stepanova & Bauer, 2021).…”

“…Substrate categories for the species in our dataset were sourced from Camaiti et al (2022). Following Stepanova and Bauer (2021), the classification was compiled based on field guides and the primary literature for each species. Species were classified into four categories, from the poorest to the richest substrates in terms of organic content: ‘sand’, ‘sandy soil’, ‘soil’, and ‘humus’.…”

“…Recent studies (Bergmann et al, 2020; Grizante et al, 2012) found significant effects of climate on body‐shape variation and evolution in squamates, linking limb reduction and body elongation with increased aridity. Substrate properties and composition may also drive lizard morphological diversity, as fossorial species live in direct contact with—or within—soil or substrate (Stepanova & Bauer, 2021), which then affects everything from their locomotion and diet to their thermal biology. This complex three‐dimensional medium can have substantial morpho‐functional implications on body‐shape evolution (e.g., relating to locomotion: Gans & Fusari, 1994; Morinaga & Bergmann, 2020).…”

A database of the morphology, ecology and literature of the world's limb‐reduced skinks

“…grass‐swimmers). These were compiled based on field guides, published conservation assessments, and the primary literature for each species, following the precedent established by Stepanova and Bauer (2021). It must be noted that this classification cannot be considered as a substitute to a precise microhabitat assessment for each species.…”