Ontogenetic allometry constrains cranial shape of the head‐first burrowing worm lizard Cynisca leucura (Squamata: Amphisbaenidae)

Abstract

Amphisbaenians are fossorial, predominantly limbless squamate reptiles with distinct cranial shapes corresponding to specific burrowing behaviors. Due to their cryptic lifestyles and the scarcity of museum specimens, little is known of their intraspecific variation, particularly regarding cranial osteology. This represents a critical lack of information, because the majority of morphological investigations of squamate relationships are based on cranial characters. We investigated cranial variation in the West African Coast Worm Lizard Cynisca leucura, a round-headed member of the Amphisbaenidae. Using geometric morphometric analyses of three-dimensional computed tomographic scans, we found that cranial osteology of C. leucura is highly conserved, with the majority of shape changes occurring during growth as the cranium becomes more slender and elongate, accompanied by increasing interdigitation among the dermal roofing bones. Elements of the ventral portion of the cranium remain loosely connected in adults, possibly as a protective mechanism against repeated compression and torsion during burrow excavation. Intraspecific variation was strongly correlated with size change from juveniles to adults, indicating a dominant role of ontogenetic allometry in determining cranial shape. We found no evidence of sexual dimorphism, either during growth or among adults. Given the fossorial habits of C. leucura, we hypothesize that cranial allometry is under strong stabilizing selection to maintain adequate proportions for head-first digging, thereby constraining the ability of individuals to respond to differing selection pressures, including sexual selection and variation in diet or microhabitat. For species in which digging imposes less mechanical stress (e.g., in softer sand), allometric associations during growth may be weakened, allowing changes to the ontogenetic trajectory and subsequent morphological traits. Such developmental dissociation between size and shape, known as heterochrony, may also be implicit in the evolution of the other amphisbaenian cranial shapes (shovel, spade, and keel), which may themselves be functionally adapted for their respective burrowing techniques. J. Morphol. 277:1159-1167, 2016. © 2016 Wiley Periodicals, Inc.

Changes in ontogenetic patterns facilitate diversification in skull shape of Australian agamid lizards

“…The weak phylogenetic signal we observe agrees with other studies on the skulls of reptiles [21, 46], mammals [47, 48], and fish [49], that have identified greater associations between morphology and diet [12, 47], feeding habits [49, 50], habitat [24, 51], and environmental factors [49, 52], than with phylogeny. In contrast, some studies confirm a strong phylogenetic signal in morphological variation, such that ecological correlations are not evident [51, 53, 54] or have minimal effect [55]. Although adaptive factors and phylogeny both undoubtedly play a role in shaping morphological diversity, the extent of this role evidently differs amongst clades and should be assessed on a case-by-case basis.…”

Skull variation in a shovel‐headed amphisbaenian genus, inferred from the geometric morphometric analysis of five South American Leposternon species

“…Gans and Montero (2008), for example, demonstrated that the large species of the (round-headed) genus Amphisbaena have skulls of a different shape in comparison with the smaller species. Magwene (1997) and Hipsley, Rentinck, Rödel, and Müller (2016) also demonstrated, respectively, significant changes in the shape of the skull of Amphisbaena caeca and Cynisca leucura during their ontogenetic development.…”

Intraspecific morphological variation in the shieldtail snakeRhinophis philippinus(Serpentes: Uropeltidae), with particular reference to tail‐shield and cranial 3D geometric morphometrics

“…Fossorial vertebrates that have reduced or no limbs have long been recognized to have accumulated cranial specializations associated with head-first burrowing. These have been studied quantitatively in taxa as diverse as caecilians (Gymnophiona: (Bardua et al, 2019;Marshall et al, 2019;Sherratt et al, 2014), worm lizards (Amphisbaenidae: (Hipsley et al, 2016), and eels (Moringuidae: (De Schepper et al, 2005). However, thus far, cranial morphology has not been investigated thoroughly or from a quantitative perspective in Uropeltidae, a major group of fossorial snakes.…”

“…Studies establishing the presence or absence of sexual dimorphism in other species of Uropeltidae could provide further tests of this possible trade-off. Among other head-first burrowing, limbless vertebrates, sexual dimorphism has been found in head or cranial shape in only some amphisbaenians (Hipsley et al, 2016) and in some caecilian amphibians. The causes and consequences are poorly understood in these typically little-studied animals.…”