Postnatal ontogeny and the evolution of macrostomy in snakes

Abstract

Macrostomy is the anatomical feature present in macrostomatan snakes that permits the ingestion of entire prey with high cross-sectional area. It depends on several anatomical traits in the skeleton and soft tissues, of which the elongation of gnathic complex and backward rotation of the quadrate represent crucial skeletal requirements. Here, the relevance of postnatal development of these skull structures and their relationship with macrohabitat and diet are explored. Contrary to the condition present in lizards and basal snakes that occupy underground macrohabitats, elements of the gnathic complex of most macrostomatan snakes that exploit surface macrohabitats display conspicuous elongation during postnatal growth, relative to the rest of the skull, as well as further backward rotation of the quadrate bone. Remarkably, several clades of small cryptozoic macrostomatans reverse these postnatal transformations and return to a diet based on prey with low cross-sectional area such as annelids, insects or elongated vertebrates, thus resembling the condition present in underground basal snakes. Dietary ontogenetic shift observed in most macrostomatan snakes is directly linked with this ontogenetic trajectory, indicating that this shift is acquired progressively as the gnathic complex elongates and the quadrate rotates backward during postnatal ontogeny. The numerous independent events of reversion in the gnathic complex and prey type choice observed in underground macrostomatans and the presence of skeletal requirements for macrostomy in extinct non-macrostomatan species reinforce the possibility that basal snakes represent underground survivors of clades that had the skeletal requirements for macrostomy. Taken together, the data presented here suggest that macrostomy has been shaped during multiple episodes of occupation of underground and surface macrohabitats throughout the evolution of snakes.

The ecological origins of snakes as revealed by skull evolution

“…Two major types of heterochronic processes—paedomorphosis and peramorphosis—have been defined in evolutionary developmental biology, but peramorphosis has been particularly hypothesized to underlie the rise of new morphologies through changes in developmental timing 52 , including an extended period (hypermorphosis), an earlier onset (predisplacement), or an increased rate of development (acceleration) of descendent lineages compared to ancestors. The regression of shape changes onto centroid size as a proxy for ontogenetic time, a widely used method to detect heterochronic trends 31 , 40 – 42 , 51 , 52 , clearly demonstrates steeper regression slopes and angles for snakes in comparison to lizards (Fig. 6a , Supplementary Fig.…”

“…The diversity in cranial structure of squamates is remarkable and appears tightly linked to functional and constructional demands within specific clades of lizards or snakes 34 – 39 , suggesting that large-scale comparisons of skull shape and size across the whole of Squamata could offer a holistic framework to address the ecological origin of snakes. Equally, cranial shape associated with ontogeny and heterochronic processes—changes in the timing and/or rate of developmental events—have been implicated in cranial evolution at different taxonomic levels in squamates 27 , 31 , 40 – 42 and other major vertebrate lineages such as mammals and archosaurs 43 , 44 . Thus far, studies tackling the evolutionary origin of snakes have largely ignored morphometric and ontogenetic information, as well as the importance of developmental mechanisms for understanding the ecological origins of snakes.…”

Exquisitely Preserved Fossil Snakes of Messel: Insight into the Evolution, Biogeography, Habitat Preferences and Sensory Ecology of Early Boas

“…Snakes of the clade Boidae (boas, anacondas, emerald boas) are arguably among the most charismatic species of living reptiles. They are one of the first offshoots of that part of the snake tree that capture and ingest prey much larger than their own head through an arsenal of anatomical and behavioural features including constriction [1], macrostomy [2], and infrared detection as an integral part of their visual system [3,4]. Boid snakes, currently distributed in the Neotropics, are part of the larger clade Booidea (Neotropical boas, "erycines", Malagasy boas, ungaliophiines and Pacific island boas), which has fuelled much debate [5][6][7][8][9] as to how a reptile group of such low apparent vagility came to be distributed across all current continents except Antarctica [10].…”

Morphological Integration and Modularity in the Hyperkinetic Feeding System of Aquatic-foraging Snakes

“…1B). Further, patterns of ontogenetic allometry in some macrostomatan snakes involve backwards rotation of the quadrate and positive allometry of the jaws, supratemporal length, and quadrate length (Scanferla 2016;Palci et al 2016), facilitating ontogenetic niche shifts in some species (Vincent et al 2007;Mushinsky 1982). This allometric axis of shape variation, affecting separate component parts (i.e., potential modules) of the snake feeding system simultaneously, has been demonstrated to be functionally consequential, evolutionary labile, and adaptive (Esquerré et al 2017, andSherratt et al 2019 report heterochronic shifts facilitating dietary shifts), suggesting that it may influence evolutionary integration within the snake skull.…”

“…, but with the quadrate and supratemporal as an individual module. The relative orientation of the quadrate varies greatly among species, which has biomechanical implications(Scanferla 2016). …”