Comparative morphology of snake (Squamata) endocasts: evidence of phylogenetic and ecological signals

Abstract

Brain endocasts obtained from computed tomography (CT) are now widely used in the field of comparative neuroanatomy. They provide an overview of the morphology of the brain and associated tissues located in the cranial cavity. Through anatomical comparisons between species, insights on the senses, the behavior, and the lifestyle can be gained. Although there are many studies dealing with mammal and bird endocasts, those performed on the brain endocasts of squamates are comparatively rare, thus limiting our understanding of their morphological variability and interpretations. Here, we provide the first comparative study of snake brain endocasts in order to bring new information about the morphology of these structures. Additionally, we test if the snake brain endocast encompasses a phylogenetic and/or an ecological signal. For this purpose, the digital endocasts of 45 snake specimens, including a wide diversity in terms of phylogeny and ecology, were digitized using CT, and compared both qualitatively and quantitatively. Snake endocasts exhibit a great variability. The different methods performed from descriptive characters, linear measurements and the outline curves provided complementary information. All these methods have shown that the shape of the snake brain endocast contains, as in mammals and birds, a phylogenetic signal but also an ecological one. Although phylogenetically related taxa share several similarities between each other, the brain endocast morphology reflects some notable ecological trends: e.g. (i) fossorial species possess both reduced optic tectum and pituitary gland; (ii) both fossorial and marine species have cerebral hemispheres poorly developed laterally; (iii) cerebral hemispheres and optic tectum are more developed in arboreal and terrestrial species.

Keywords: brain endocast; computed tomography; ecological signal; morphometrics; sensory information; snakes; squamates.

Figure 1

Schematic phylogenetic relationships of snakes sampled in the study (modified from Lee & Scanlon, 2002; Pyron et al. 2011; Hsiang et al. 2015, 2002). Principal ecology/habitat: fossorial (f), terrestrial (t), arboreal (a), semi‐aquatic (sa), marine (m).

Figure 2

Reconstructed brain endocast of Enhydris punctata (Homalopsidae). (A) Illustration of the major structures seen in dorsal and left lateral views: telencephalon (red), diencephalon (yellow), mesencephalon (green), rhombencephalon (purple). (B) Illustration of the various measurements defined in Materials and methods, and taken in dorsal, left lateral and ventral views. fr‐p, fronto‐parietal suture; lim, groove between the optic tectum and the cerebral hemispheres; p‐pr‐bs, triple point formed by the sutures between the parietal, prootic and basisphenoid; p‐so, parietal‐supraoccipital suture; pr‐bs‐bo, triple point formed by the suture between the prootic, basisphenoid and basioccipital; so‐eo, supraoccipital‐exoccipital suture; so‐pr‐eo, triple point formed by the sutures of the supraoccipital, prootic and exoocipital; DWPE, dorsal width of the posterior end of the brain endocast; HCH, maximal height of the cerebral hemisphere; HOB, height of the main olfactory bulb; HOP, height of the olfactory peduncle; HOR, height of the optic tectum; HP, height of the pituitary bulb; HPE, height of the posterior part of the brain endocast; LCH, lateral expansion of the cerebral hemispheres; LE, length of the brain endocast; LFI, length of the interhemispheric fissure; LG, length of the groove between olfactory bulbs; LOB, length of the olfactory bulbs; LOR, length of the optic tectum; LP, length of the pituitary bulb; LPE, length of the posterior part of the brain endocast; WCH, maximal width of the cerebral hemispheres; WIE, width of the inner ear region; WOP, width of the olfactory peduncles; WOR, maximal width of the optic tectum; WP, width in the pituitary gland region; WPE, width of the ventral part of the brain endocast. Scale bar: 2 mm.

Figure 3

Skull of Enhydris punctata (Homalopsidae) in dorsal (A) and left lateral (B) views showing the bones surrounding the brain endocast; (C,D) with bones rendered transparent to reveal the brain endocast (green) and the inner ear (red). bo, basioccipital; bs, basisphenoid; eo, exoccipitals; fr, frontal; p, parietal; pr, prootics; so, supraoccipitals. Scale bar: 2 mm.

Figure 4

Brain endocasts in dorsal view of (A) Typhlophys squamosus (Typhlopidae); (B) Hierophis viridiflavus (Colubridae); (C) Cylindrophis ruffus (Cylindrophiidae); (D) Acrochordus granulatus (Acrochordidae); (E) Eunectes murinus (Boidae); (F) Homalopsis buccata (Homalopsidae); (G) Chrysopelea ornata (Colubridae); (H) Anilius scytale (Aniliidae). Scale bars: 1 mm.

Figure 5

Brain endocasts in left lateral view of (A) Typhlophys squamosus (Typhlopidae); (B) Boiga dendrophila (Colubridae); (C) Homalopsis buccata (Homalopsidae); (D) Mimophis mahfalensis (Lamprophiidae); (E) Anilius scytale (Aniliidae); (F) Hierophis viridiflavus (Colubridae); (G) Eunectes murinus (Boidae); (H) Enhydrina schistosa (Elapidae); (I) Dispholidus typus (Colubridae); (J) Thamnophis sirtalis (Natricidae). Scale bars: 1 mm.

Figure 6

Brain endocasts in dorsal (upper row) and left lateral (lower row) views of (A) Thamnophis sirtalis (Natricidae); (B) Erpeton tentaculatum (Homalopsidae); (C) Hydrophis major (Elapidae); (D) Erpeton tentaculatum. Scale bars: 1 mm.

Figure 7

Brain endocasts in left lateral view of (A) Boa constrictor (Boidae); (B) Crotalus atrox (Viperidae). Scale bars: 1 mm.

Figure 8

Results of the PCoA performed on the snake brain endocast characters (Appendix S3). See Table 1 for name abbreviations.

Figure 9

Results of the PCA performed on the brain endocast variables for three Python regius specimens, (P1) smaller specimen, (P3) intermediate specimen, (P2) largest specimen. Scatter plot illustrating the position of the different specimens on the first two principal components. DWPE, dorsal width of the posterior end of the brain endocast; HCH, maximal height of the cerebral hemisphere; HOB, height of the main olfactory bulb; HOP, height of the olfactory peduncle; HOR, height of the optic tectum; HP, height of the pituitary bulb; HPE, height of the posterior part of the brain endocast; LCH, lateral expansion of the cerebral hemispheres; LE, length of the brain endocast; LFI, length of the interhemispheric fissure; LG, length of the groove between olfactory bulbs; LOB, length of the olfactory bulbs; LOR, length of the optic tectum; LP, length of the pituitary gland; LPE, length of the posterior part of the brain endocast; WCH, maximal width of the cerebral hemispheres; WIE, width in the inner ear region; WOP, width of the olfactory peduncles; WOR, maximal width of the optic tectum; WP, width in the pituitary gland region; WPE, width of the ventral part of the brain endocast.

Figure 10

Results of the PCAs performed on the snake brain endocast variables of the 45 specimens. Scatter plot illustrating the position of the different species on the first and second principal components and figuring the different ecologies. See Table 1 for name abbreviations.

Figure 11

Results of the PCAs performed on the snake brain endocast outline curves in ventral view. The blue and dark dotted lines indicate, respectively, the low and high values along the two axes. See Table 1 for name abbreviations.

Figure 12

Results of the PCAs performed on the snake brain endocast outline curves in lateral view. The blue and dark dotted lines indicate, respectively, the low and high values along the two axes. See Table 1 for name abbreviations.