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.

Keywords: evolution; macrostomy; postnatal ontogeny; snakes.

Figure 1.

Postnatal transformations in the gnathic complex in lizards and snakes. (a) Juvenile (SVL 56 mm) and adult (SVL 237 mm) of the anguid lizard Ophiodes intermedius; (b) juvenile (SVL 43 mm) and adult (SVL 131 mm) of the typhlopid scolecophidian snake Amerotyphlops brongersmianus; (c) juvenile (SVL 212 mm) and adult (SVL 895 mm) of the basal alethinophidian snake Anilius scytale; (d) juvenile (SVL 311 mm) and adult (SVL 1620 mm) of the macrostomatan snake Boa constrictor.

Figure 2.

Postnatal transformations in the gnathic complex of cryptozoic macrostomatans. (a) Lateral view of the skull of a juvenile (SVL 114 mm) and adult (SVL 277 mm) of the dipsadine colubroid Atractus reticulatus; (b) juvenile (SVL 182 mm) and adult (SVL 921 mm) of the elapid Micrurus pyrrhocryptus. Scale bars, 2 mm.

Figure 3.

Metrics of changes in underground and surface snake gnathic complex elements during postnatal ontogeny.

Figure 4.

Rotation of the quadrate bone during postnatal development in the macrostomatan snake Boa constrictor. (a) Late embryo (SVL 299 mm); (b) hatchling (SVL 311 mm); (c) juvenile (SVL 463 mm); (d) adult (SVL 1620 mm). Not to scale.

Figure 5.

Graphical summary of the ecological morphological survey performed between body size (SVL), prey type and macrohabitat preferences of a set of adult extant snakes. Each point represents one species and points joined by a dotted line represent a single species with two prey type preferences.

Figure 6.

Simplified phylogenetic tree of snakes [45] showing the information discussed in this work about body size, macrohabitat, prey type preferences and osteological requirements for macrostomy. Note the early appearance of crucial osteological requirements for macrostomy and the elongation of the gnathic complex present in non-macrostomatan simoliophiids.