Skip to main content
Erschienen in: Brain Structure and Function 7/2021

21.07.2021 | Original Article

Inside the head of snakes: influence of size, phylogeny, and sensory ecology on endocranium morphology

verfasst von: Marion Segall, Raphaël Cornette, Arne R. Rasmussen, Christopher J. Raxworthy

Erschienen in: Brain Structure and Function | Ausgabe 7/2021

Einloggen, um Zugang zu erhalten

Abstract

Environmental properties, and the behavioral habits of species impact sensory cues available for foraging, predator avoidance and inter/intraspecific communication. Consequently, relationships have been discovered between the sensory ecology and brain morphology in many groups of vertebrates. However, these types of studies have remained scare on snake. Here, we investigate the link between endocranial shape and the sensory-related ecology of snakes by comparing 36 species of snakes for which we gathered six sensory-ecology characteristics. We use µCT scanning and 3D geometric morphometrics to compare their endocranium in a phylogenetically informed context. Our results demonstrate that size is a major driver of endocranial shape, with smaller species tending to maximize endocranial volume using a more bulbous shape, while larger species share an elongate endocranial morphology. Phylogeny plays a secondary role with more derived snakes diverging the most in endocranial shape, compared to other species. The activity period influences the shape of the olfactory and optic tract, while the foraging habitat impacts the shape of the cerebellum and cranial nerve regions: structures involved in orientation, equilibrium, and sensory information. However, we found that endocranial morphology alone is not sufficient to predict the activity period of a species without prior knowledge of its phylogenetic relationship. Our results thus demonstrate the value of utilizing endocranial shape as complementary information to size and volume in neurobiological studies.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat Adams DC, Collyer ML, Kaliontzopoulou A (2020) Package “geomorph”, pp 1–140 Adams DC, Collyer ML, Kaliontzopoulou A (2020) Package “geomorph”, pp 1–140
Zurück zum Zitat Balanoff AM, Bever GS (2017) The role of endocasts in the study of brain evolution. In: Kaas JH (ed) Evolution of nervous systems, Academic Press, pp 223–241 Balanoff AM, Bever GS (2017) The role of endocasts in the study of brain evolution. In: Kaas JH (ed) Evolution of nervous systems, Academic Press, pp 223–241
Zurück zum Zitat Bertrand OC, San Martin-Flores G, Silcox MT (2019) Endocranial shape variation in the squirrel-related clade and their fossil relatives using 3D geometric morphometrics: contributions of locomotion and phylogeny to brain shape. J Zool 308:197–211. https://doi.org/10.1111/jzo.12665CrossRef Bertrand OC, San Martin-Flores G, Silcox MT (2019) Endocranial shape variation in the squirrel-related clade and their fossil relatives using 3D geometric morphometrics: contributions of locomotion and phylogeny to brain shape. J Zool 308:197–211. https://​doi.​org/​10.​1111/​jzo.​12665CrossRef
Zurück zum Zitat Burghardt GM, Ford NB (1993) Perceptual mechanisms and the behavioral ecology of snakes. Snakes: ecology and behavior. The Blackburn Press, New Jersey, pp 117–164 Burghardt GM, Ford NB (1993) Perceptual mechanisms and the behavioral ecology of snakes. Snakes: ecology and behavior. The Blackburn Press, New Jersey, pp 117–164
Zurück zum Zitat Camilleri C, Shine R (1990a) Sexual dimorphism and dietary divergence : differences in trophic morphology between male and female snakes. Copeia 1990:649–658CrossRef Camilleri C, Shine R (1990a) Sexual dimorphism and dietary divergence : differences in trophic morphology between male and female snakes. Copeia 1990:649–658CrossRef
Zurück zum Zitat Cooper WEJ (2008) Tandem evolution of diet and chemosensory responses in snakes. Amphibia-Reptilia 29:393–398CrossRef Cooper WEJ (2008) Tandem evolution of diet and chemosensory responses in snakes. Amphibia-Reptilia 29:393–398CrossRef
Zurück zum Zitat Czaplicki JA, Porter RH (1974) Visual cues mediating the selection of goldfish (Carassius auratus) by two species of Natrix. J Herpetol 8:129–134CrossRef Czaplicki JA, Porter RH (1974) Visual cues mediating the selection of goldfish (Carassius auratus) by two species of Natrix. J Herpetol 8:129–134CrossRef
Zurück zum Zitat De Cock BT (1983) Thermal sensitivity as a specialization for prey capture and feeding in snakes. Am Zool 23:363–375CrossRef De Cock BT (1983) Thermal sensitivity as a specialization for prey capture and feeding in snakes. Am Zool 23:363–375CrossRef
Zurück zum Zitat Franz R (1977) Observations on the food, feeding behavior, and parasites of the striped swamp snake, Regina alleni. Herpetologica 33:91–94 Franz R (1977) Observations on the food, feeding behavior, and parasites of the striped swamp snake, Regina alleni. Herpetologica 33:91–94
Zurück zum Zitat Heatwole H (1999) Sea snakes. University of New South Wales Press Ltd, Kensington Heatwole H (1999) Sea snakes. University of New South Wales Press Ltd, Kensington
Zurück zum Zitat Iwaniuk AN (2017) Functional correlates of brain and brain region sizes in nonmammalian vertebrates. In: Kaas JH (ed) Evolution of nervous systems, Academic Press, pp 335–348 Iwaniuk AN (2017) Functional correlates of brain and brain region sizes in nonmammalian vertebrates. In: Kaas JH (ed) Evolution of nervous systems, Academic Press, pp 335–348
Zurück zum Zitat Jayne BC, Voris HK, Ng PKL (2002) Snake circumvents constraints on prey size. Nature 418:143CrossRef Jayne BC, Voris HK, Ng PKL (2002) Snake circumvents constraints on prey size. Nature 418:143CrossRef
Zurück zum Zitat Kaas JH (2017) Evolution of nervous systems, 2nd edn. Academic Press Kaas JH (2017) Evolution of nervous systems, 2nd edn. Academic Press
Zurück zum Zitat Kropach CN (1975) The yellow-bellied sea snake, Pelamis, in the eastern Pacific. In: Dunson WA (ed) The biology of sea snakes. University Park Press, Baltimore, pp 185–213 Kropach CN (1975) The yellow-bellied sea snake, Pelamis, in the eastern Pacific. In: Dunson WA (ed) The biology of sea snakes. University Park Press, Baltimore, pp 185–213
Zurück zum Zitat Lebrun R (2017) ISE-MeshTools v1.3.4. pp 1–101 Lebrun R (2017) ISE-MeshTools v1.3.4. pp 1–101
Zurück zum Zitat Moon BR, Penning DA, Segall M, Herrel A (2019) Feeding in snakes: form, function, and evolution of the feeding system. In: Bels V, Whishaw IQ (eds) Feeding in vertebrates: evolution, morphology, behavior, biomechanics. Springer Nature, Switzerland, pp 528–574 Moon BR, Penning DA, Segall M, Herrel A (2019) Feeding in snakes: form, function, and evolution of the feeding system. In: Bels V, Whishaw IQ (eds) Feeding in vertebrates: evolution, morphology, behavior, biomechanics. Springer Nature, Switzerland, pp 528–574
Zurück zum Zitat Nieuwenhuys R, ten Donkelaar HJ, Nicholson C (1998) The central nervous system of vertebrates. Springer, BerlinCrossRef Nieuwenhuys R, ten Donkelaar HJ, Nicholson C (1998) The central nervous system of vertebrates. Springer, BerlinCrossRef
Zurück zum Zitat Noonloy T, Kunya K, Chanhome L et al (2018) Crab-ripping: an unusual feeding behavior newly recorded in freshwater snakes. Bull Chicago Herpetol Soc 53:53–56 Noonloy T, Kunya K, Chanhome L et al (2018) Crab-ripping: an unusual feeding behavior newly recorded in freshwater snakes. Bull Chicago Herpetol Soc 53:53–56
Zurück zum Zitat Pedersen TL, Crameri F (2020) Package “scico”, pp 1–7 Pedersen TL, Crameri F (2020) Package “scico”, pp 1–7
Zurück zum Zitat Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things), pp 217–223 Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things), pp 217–223
Zurück zum Zitat Ripley B, Venables W (2020) Package ‘class’, pp 1–19 Ripley B, Venables W (2020) Package ‘class’, pp 1–19
Zurück zum Zitat Schaeffel F, de Queiroz A (1990) Alternative mechanisms of enhanced underwater vision in the garter snakes Thamnophis melanogaster and T. couchii. Copeia 1990:50–58CrossRef Schaeffel F, de Queiroz A (1990) Alternative mechanisms of enhanced underwater vision in the garter snakes Thamnophis melanogaster and T. couchii. Copeia 1990:50–58CrossRef
Zurück zum Zitat Schlager S (2017) Morpho and Rvcg–Shape analysis in R: R-Packages for geometric morphometrics, shape analysis and surface manipulations. In: Zheng G, Li S, Szekely G (eds) Statistical shape and deformation analysis: methods implementation and applications. Academic Press, pp 217–256CrossRef Schlager S (2017) Morpho and Rvcg–Shape analysis in R: R-Packages for geometric morphometrics, shape analysis and surface manipulations. In: Zheng G, Li S, Szekely G (eds) Statistical shape and deformation analysis: methods implementation and applications. Academic Press, pp 217–256CrossRef
Zurück zum Zitat Schwenk K (2008) Comparative anatomy and physiology of chemical senses in nonavian aquatic reptiles. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold adaptations in secondarily aquatic vertebrates. University of California Press, pp 65–81 Schwenk K (2008) Comparative anatomy and physiology of chemical senses in nonavian aquatic reptiles. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold adaptations in secondarily aquatic vertebrates. University of California Press, pp 65–81
Zurück zum Zitat Starck D (1979) Cranio-cerebral relations in recent reptiles. Biology of the reptilia, 9 neurology A. Academic Press Inc. Ltd, London, pp 1–38 Starck D (1979) Cranio-cerebral relations in recent reptiles. Biology of the reptilia, 9 neurology A. Academic Press Inc. Ltd, London, pp 1–38
Zurück zum Zitat Stevens M (2013) Sensory ecology, behavior, and evolution. Oxford University Press, OxfordCrossRef Stevens M (2013) Sensory ecology, behavior, and evolution. Oxford University Press, OxfordCrossRef
Zurück zum Zitat Thewissen JGM, Nummela S (2008) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, LondonCrossRef Thewissen JGM, Nummela S (2008) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, LondonCrossRef
Zurück zum Zitat Voris HK, Voris HH, Liat LB (1978) The food and feeding behavior of a marine snake, Enhydrina schistosa (Hydrophiidae). Copeia 1978:134–146CrossRef Voris HK, Voris HH, Liat LB (1978) The food and feeding behavior of a marine snake, Enhydrina schistosa (Hydrophiidae). Copeia 1978:134–146CrossRef
Zurück zum Zitat Yopak KE, Pakan JMP, Wylie D (2017) The cerebellum of nonmammalian vertebrates. In: Evolution of nervous systems, 2nd edn, Elsevier, pp 373–385 Yopak KE, Pakan JMP, Wylie D (2017) The cerebellum of nonmammalian vertebrates. In: Evolution of nervous systems, 2nd edn, Elsevier, pp 373–385
Zurück zum Zitat Young BA (2007) Response of the yellow anaconda (Eunectes notaeus) to aquatic acoustic stimuli. In: Henderson RW, Powell R (eds) Biology of the boas and pythons. Eagle Mountain Publishing, Utah, pp 199–205 Young BA (2007) Response of the yellow anaconda (Eunectes notaeus) to aquatic acoustic stimuli. In: Henderson RW, Powell R (eds) Biology of the boas and pythons. Eagle Mountain Publishing, Utah, pp 199–205
Metadaten
Titel
Inside the head of snakes: influence of size, phylogeny, and sensory ecology on endocranium morphology
verfasst von
Marion Segall
Raphaël Cornette
Arne R. Rasmussen
Christopher J. Raxworthy
Publikationsdatum
21.07.2021
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 7/2021
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-021-02340-6

Weitere Artikel der Ausgabe 7/2021

Brain Structure and Function 7/2021 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.