Postnatal ontogeny and the evolution of macrostomy in snakes

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.


Three-dimentional reconstructions based on HRXCT data
Comparative specimens available from the Digital Morphology Library at the semifossorial, semiaquatic) that introduced more confusion. Regrettably, this situation entails the negative consequence of hinder comparisons between macrohabitats and their evolutionary implications for species that occupy them. Hence, I provide an explicit terminology that imparts each macrohabitat with information about its anatomical correlates in snakes. However, a caveat must be made because some snakes are capable to occupy different macrohabitats without specific anatomical structures. A good example of this situation is the arboreal capabilities of several snakes, even present in fossorial scolecophidians of the family Leptotyphlopidae (Vanzolini, 1970;pers. obs.). This attempt is based on previous works that employed macrohabitat definitions, in special the papers of Duellman (1978), Cadle and Greene (1993) and Martins and Oliveira (1998).

Underground macrohabitats
It is important to note that most snakes are facultatively sheltering due to the ecological plasticity of their elongated limbless bauplan. Despite of this plastic condition, some groups display habitat specializations, which usually are correlated with discrete anatomical traits. Most basal groups of snakes and some groups of macrostomatans inhabit in tunnels, crevices or below of different strata composed by many kinds of leaf litters and other loose substrates present in poorly consolidated substrates. Common among snakes that occupy underground macrohabitats is the small body size (SVL < 1000 mm), strong to moderate reduction of eyes and consequently orbits, reduction of the number of dorsal scale rows, fusion of head scales and strong abbreviation of the tail (Bogert, 1947;Inger and Marx, 1965;Downs, 1967;Gans, 1974;Shine and Wall, 2008). Because head is the principal locomotor organ in this kind of snakes, head morphology is strongly constrained due to the ability to penetrate the substrate and exposure of cranial bones to stress. Head width also may be reduced and cranial rigidity increased by shortening the supratemporals and quadrates whit the subsequent shortening of the lower jaws, robustness and shape modification of the premaxilla bone and naso-frontal joint, narrowing of the braincase and rearrangement of muscular and glandular elements (Gans, 1974;Savitzky, 1978Savitzky, , 1983. Associated with the reduction of body diameter, neural spines are strongly reduced or absent (Johnson, 1955).

Fossorial (=burrowing, subterranean, active burrower)
Fossorial snakes are those capable of burrowing and/or using soil galleries and regularly spend their activity time in the soil. I consider truly fossorial snakes all scolecophidians and basal alethinophidian such as uropeltids and species of the genus Anomochilus. These snakes exhibit strong body modifications such as rigid skull and very narrow heads (usually both body extremes are similar in shape), strongly reduced eyes covered by a scale and modifications in the caudal scalation to form tail shields or spines. Nearly all species of these groups have thin, small bodies (SVL < 600 mm), and a homogeneous cylindrical body shape.

Surface macrohabitats
Snakes that occupy surface macrohabitats display an important range of body sizes (SVL ≈ or > 1000 mm) including large forms that can reach several meters.
Surface snakes spend most part of their activity time above the substrate, climbing plants or in the water column. Due to the relevance of the postcranial body as locomotor organ in surface snakes, exist some anatomical traits related with the different surface macrohabitats. Related with the increase of body size, surface snakes have more vertebrae than underground snakes (Lindell, 1994). It is important to note that few taxa exhibit characters present in underground forms. An example of this is the shortening of the suspensorium and jaws present in presumably paedomorphic surface snakes such as some boine species of the genus Chilabothrus (Kluge, 1989).

Terrestrial (= ground inhabitants, surface-dwelling)
Terrestrial snakes are those that regularly spend this activity time on the ground, above to different kind of substrates (leaf litter, sand, rocks, etc). Terrestrial snakes display the most generalised forms with respect of body shape. It is important to underline that largest snake species (SVL > 3000 mm) occupy this macrohabitat.

Arboreal (=bush and tree inhabitants)
Arboreal snakes are those that regularly spend part of their activity time on the vegetation (epiphytes, vines, shrubs and trees) above the ground level (Martins and Oliveira, 1999). Their body is usually slender and thin, and usually tail is more slender than terrestrial or aquatic forms (Marx and Rabb, 1972;Lillywhite and Henderson, 1993;Lindell, 1994). Usually, arboreal forms have more precloacal vertebrae than terrestrial and aquatic forms, and some species of colubroids (e.g. Leptophis ahaetula) have elongated vertebral centra.

Aquatic (=water snakes, marine snakes)
Aquatic indicates those snakes that regularly spend part of their activity time inside the water. Some freshwater forms like the boid Eunectes, homalopsine and hydropsine colubroids show external nares and eyes in the dorsal region of the head.
Sea snakes exhibit a dorso-ventrally elongated body (due to a prominent ventral keel), and the tail (a major propulsive structure during swimming) is higher and thinner than in terrestrial snakes (i.e., paddle-shaped) but shorter relative to body length (Brischoux and Shine, 2011). Simoliophiids were fossil Mesozoic snakes recovered invariably in marine sedimentary formations, which display some particular postcranial traits usually attributed to a marine habitat such as pronounced pachyostosis in vertebrae and ribs (Lee and Caldwell, 1998;Rieppel et al., 2003;Rage and Escuillié, 2000), and elongated haemal arches in postcloacal region (but see Rieppel and Head [2006] for the homology status of these caudal structures).

D. Prey types
This definition of prey types is reproduced with some modifications from the classical work of Cundall and Greene (2000) about snake feeding.

Type I
Preys of this type consist on relatively small items in mass and cross-sectional area regardless of shape, such as adult insects and their different developmental stages (pupae, larvae), fish eggs, among others.

Type II
Type II preys are elongate, often without protruding locomotor organs like arthropod appendages or tetrapod limbs. I include in this category earthworms, elongated fishes, legless tetrapods, small elongated legged lizards and soft-shelled squamate eggs. This kind of preys has a small cross-sectional area.

Type III
Type III prey are fusiform or roughly spherical as well as relatively heavy so they necessitate compensation for both high handling cost and increased gape. We incorporate large lizards in this category.

Type IV
Type IV prey weigh substantially less than predicted by their maximum diameter, either because their cross-sectional shape is not circular (e.g., many fishes) or they possess protruding body parts (e.g. wings of birds and bats) so they require large gape but not specialized immobilization mechanisms.