Yinmeng HOU,Xiaoxiao SHU,Shengchao SHI,et al.Endocast Morphological Variation and Its Driving Forces in Scutiger boulengeri[J].Asian Herpetological Research(AHR),2022,13(4):269-283.[doi:10.16373/j.cnki.ahr.220005]
Click Copy

Endocast Morphological Variation and Its Driving Forces in Scutiger boulengeri
Share To:

Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

2022 VoI.13 No.4
Research Field:
Publishing date:


Endocast Morphological Variation and Its Driving Forces in Scutiger boulengeri
Yinmeng HOU123 Xiaoxiao SHU123 Shengchao SHI123 Xiuqin LIN13 Luyao XIAO13 Jianping JIANG134 Jianghong RAN2 and Feng XIE13*
1 CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization, Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, Sichuan, China
2 College of Life Sciences, Sichuan University, Chengdu 610065, Sichuan, China
3 University of the Chinese Academy of Sciences, Beijing 100049, China
4 Mangkang Biodiversity and Ecological Station, Tibet Ecological Safety Monitor Network, Changdu 854500, Tibet, China
aquatic preference cranial endocast ecological adaptation phylogenetic history shape variation
Cranial endocasts can be used as a reliable proxy for brain size, reflecting the evolutionary and environmental selection pressure of species. Although studies on endocasts in amphibians have increased in recent years, those performed on endocasts of Anura are comparatively rare, especially at the intraspecific level. Here, using a high-altitude endemic toad—Scutiger boulengeri—as a model, through the application of integrative methods (morphology, anatomy, phylogeny, and ecology), we studied intraspecific variations in endocast morphology and explored its driving forces. Three-dimensional reconstruction and the brain-to-endocranial cavity (BEC) index suggested that the endocast of S. boulengeri can reflect brain morphology to a large extent. Elliptic Fourier analysis and principal component analysis revealed great variability in the cranial endocast morphology among individuals, as well as the variation concentrated in the regions of telencephalon and optic tectum. In the species, individuals with large bodies are accompanied by a larger endocast size; the relative endocast sizes have significant clade differences but no sexual dimorphism. Additionally, the relative endocast sizes of S. boulengeri were not associated with phylogenetic history and aquatic preference but were positively correlated with altitude and negatively correlated with oxygen content, temperature, and precipitation factors (annual mean temperature, temperature seasonality, annual precipitation, and precipitation seasonality). These findings suggested that high-altitude and extreme environmental conditions acted as important selective forces in morphological variation of the cranial endocast of S. boulengeri.


Abràmoff M. D., Magalh?es P. J., Ram S. J. 2004. Image processing with ImageJ. Biophoton Int, 11(7): 36–42
Adams D. C. 2014. A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Syst Biol, 63: 685–697
Allemand R., Boistel R., Daghfous G., Blanchet Z., Cornette R., Bardet N., Vincent P., Houssaye A. 2017. Comparative morphology of snake (Squamata) endocasts: evidence of phylogenetic and ecological signals. J Anat, 231: 849–868
Allemand R., Houssaye A., Bardet N., Vincent P. 2019. Endocranial anatomy of plesiosaurians (Reptilia, Plesiosauria) from the Late Cretaceous (Turonian) of Goulmima (southern Morocco). J Vertebr Paleontol, 39(2): e1595636
Amiel J. J., Tingley R., Shine R. 2011. Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles. PLoS One, 6: e18277
Axelrod C. J., Laberge F., Robinson B. W. 2018. Intraspecific brain size variation between coexisting sunfish ecotypes. Proc R Soc B, 285: 20181971
Axelrod C. J., Laberge F., Robinson B. W. 2021. Interspecific and intraspecific comparisons reveal the importance of evolutionary context in sunfish brain form divergence. J Evol Biol, 34(4): 639–652
Badyaev A. V., Ghalambor C. K. 2001. Evolution of life histories along elevational gradients: Trade-off between parental care and fecundity. Ecology, 82: 2948–2960
Balanoff A. M., Bever G. S. 2020. Chapter 3–The Role of Endocasts in the Study of Brain Evolution. In Kaas J. H. (Ed.), Evolutionary Neuroscience (Second Edition). New York: Academic Press, 29–49
Balanoff A. M., Bever G. S., Ikejiri T. 2010. The braincase of Apatosaurus (Dinosauria: Sauropoda) based on computed tomography of a new specimen with comments on variation and evolution in sauropod neuroanatomy. Am Mus Novit, 3677: 1–32
Beckmann M., Václavík T., Manceur A. M., ?prtová L., Wehrden H. V., Welk E., Cord A. F. 2014. glUV: A global UV-B radiation data set for macroecological studies. Methods Ecol Evol, 5: 372–383
Bedriaga J. V. 1898. Amphibien und Reptilien. Wissenschaftliche Resultate der von N. M. Przewalski nach Central-Asien unternommenen Reisen, & c./Nauchnuie Rezul’tatui puteshestvii N. M. Przh’skagho po tzentral’noi Azii, & c. Vol. 3, Zoologischer Theil, Part 1: St. Petersburg, Akadamie der Wissenschaften
Beltz B. S. 2019. Brain Evolution: Adaptations to extreme conditions. Elife, 8: e50647
Blomberg S. P., Garland Jr T., Ives A. R. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57(4): 717–745
Challands T., Pardo J. D., Clement A. M. 2020. Mandibular musculature constrains brain–endocast disparity between sarcopterygians. R Soc Open Sci, 7(9): 200933
Chown S. L., Klok C. J. 2003. Altitudinal body size clines: latitudinal effects associated with changing seasonality. Ecography, 26(4): 445–455
Chen W., Bi K., Fu J. Z. 2009. Frequent mitochondrial gene introgression among high elevation Tibetan megophryid frogs revealed by conflicting gene genealogies. Mol Ecol, 18(13): 2856–2876
Clement A. M., Mensforth C. L., Challands T., Collin S. P., Long J. A. 2021. Brain Reconstruction Across the Fish-Tetrapod Transition; Insights From Modern Amphibians. Front Ecol Evol, 9: 160
Clement A. M., Nysj? J., Strand R., Ahlberg P. E. 2015. Brain–endocast relationship in the Australian lungfish, Neoceratodus forsteri, elucidated from tomographic data (Sarcopterygii: Dipnoi). PLoS One, 10(10): e0141277
Clement A. M., Strand R., Nysj? J., Long J. A., Ahlberg P. E. 2016. A new method for reconstructing brain morphology: Applying the brain-neurocranial spatial relationship in an extant lungfish to a fossil endocast. R Soc Open Sci, 3(7): 160307
Drummond A. J., Suchard M. A., Xie D., Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol, 29(8): 1969–1973
Dunbar R. I. 1998. The social brain hypothesis. Evol Anthropol, 6(5): 178–190
Favre A., Paeckert M., Pauls S. U., Jaehnig S. C., Uhl D., Michalak I., Muellner-Riehl A. N. 2015. The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biol Rev Camb Philos Soc, 90: 236–253
Fei L., Hu S. Q., Ye C. Y., Huang Y. Z. 2009. Fauna Sinica, Amphibia, Vol. 2, Anura. Beijing: Science Press, 957pp (In Chinese)
Fei L., Ye C. Y. 1987. Comparative studies on skeleton of twelve species of pelobatid toad (Genus Scutiger, Anura: Pelobatidae) from Qinghai-Xizang Plateau. Acta Biol Plateau Sinica, 7: 155–170 (In Chinese)
Fick S. E., Hijmans R. J. 2017. WorldClim 2: New 1‐km spatial resolution climate surfaces for global land areas. Int J Climatol, 37(12): 4302–4315
Finarelli J. A. 2006. Estimation of endocranial volume through the use of external skull measures in the Carnivora (Mammalia). J Mammal, 87(5): 1027–1036
Fitzpatrick J., Almbro M., Gonzalez-Voyer A., Hamada S., Pennington C., Scanlan J., Kolm N. 2012. Sexual selection uncouples the evolution of brain and body size in pinnipeds. J Evol Biol, 25(7): 1321–1330
Foth C., Evers S. W., Joyce W. G., Volpato V. S., Benson R. B. 2019. Comparative analysis of the shape and size of the middle ear cavity of turtles reveals no correlation with habitat ecology. J Anat, 235(6): 1078–1097
Garamszegi L. Z., Eens M., Erritz?e J., M?ller A. P. 2005. Sexually size dimorphic brains and song complexity in passerine birds. Behav Ecol, 16(2): 335–345
Gonda A, Herczeg G, Meril? J. 2013. Evolutionary ecology of intraspecific brain size variation: A review. Ecol Evol, 3(8): 2751–2764
Haines A. J., Crampton J. S. 2000. Improvements to the method of Fourier shape analysis as applied in morphometric studies. Palaeontology, 43(4): 765–783
Harvey P. H., Krebs J. R. 1990. Comparing brains. Science, 249(4965): 140–146
Hijmans R. J., Cameron S. E., Parra J. L., Jones P. G., Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol, 25(15): 1965–1978
Hofmann S., St?ck M., Zheng Y., Ficetola F.G., Li J. T., Scheidt U., Schmidt J. 2017. Molecular phylogenies indicate a Paleo-Tibetan origin of Himalayan lazy toads (Scutiger). Sci Rep, 7(1): 1–12
Huang Y., Mai C. L., Liao W. B., Kotrschal A. 2020. Body mass variation is negatively associated with brain size: Evidence for the fat‐brain trade‐off in anurans. Evolution, 74(7): 1551–1557
Isler K., van Schaik C. P. 2012. Allomaternal care, life history and brain size evolution in mammals. J Hum Evol, 63: 52–63
Hurlburt G. R., Ridgely R. C., Witmer L. M. 2013. Relative size of brain and cerebrum in tyrannosaurid dinosaurs: An analysis using brain-endocast quantitative relationships in extant alligators. Tyrannosaurid paleobiology, 1–21
Iwaniuk A. N., Nelson J. E. 2002. Can endocranial volume be used as an estimate of brain size in birds? Can J Zool, 80(1): 16–23
Iwata H., Ukai Y. 2002. SHAPE: A computer program package for quantitative uation of biological shapes based on elliptic Fourier descriptors. J Hered, 93(5): 384–385
Jerison H. J. 2009. Allometric Analysis of Brain Size. Encyclopedia of Neuroscience, 239–244
Klecka W. R. 1980. Discriminant analysis. Newbury Park, London, New Delhi: Sage Publications, 69 pp
Kotrschal K., Van Staaden M., Huber R. 1998. Fish brains: Evolution and anvironmental relationships. Rev Fish Biol Fish, 8(4): 373–408
Kumar S., Stecher G., Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol, 33(7): 1870–1874
Lanfear R., Frandsen P. B., Wright A. M., Senfeld T., Calcott B. 2017. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol, 34(3): 772–773
Li R., Chen W., Tu L., Fu J. Z. 2009. Rivers as barriers for high elevation amphibians: A phylogeographic analysis of the alpine stream frog of the Hengduan Mountains. J Zool, 277(4): 309–316
Liao J., Liu N. 2008. Altitudinal variations of acoustic organs in anurans: A case study from China. Ital J Zool, 75(2): 125–134
Liao W. B., Lou S. L., Zeng Y., Meril? J. 2015. Evolution of anuran brains: Disentangling ecological and phylogenetic sources of variation. J Evol Biol, 28: 1986–1996
Lin X. Q., Shih C., Hou Y. M., Shu X. X., Zhang M. H., Hu J. H., Jiang J. P., Xie F. 2021. Climatic-niche evolution with key morphological innovations across clades within Scutiger boulengeri (Anura: Megophryidae). Ecol Evol, 11: 10353–10368
Lovich J. E., Gibbons J. W. 1992. A review of techniques for quantifying sexual size dimorphism. Growth Dev Aging, 56: 269–281
Lu A., Kang S., Li Z., Theakstone W. H. 2010. Altitude effects of climatic variation on Tibetan Plateau and its vicinities. J Earth Sci, 21(2): 189–198
Luo Y., Zhong M. J., Huang Y., Li F., Liao W. B., Kotrschal, A. 2017. Seasonality and brain size are negatively associated in frogs: Evidence for the expensive brain framework. Sci Rep, 7: 1–9
Mai C. L., Liao W. B., Kotrschal A., Lüpold S. 2020. Relative brain size is predicted by the intensity of intrasexual competition in frogs. Am Nat, 196(2): 69–179
Marcucio R. S., Young N. M., Hu D., Hallgrimsson B. 2011. Mechanisms that underlie co‐variation of the brain and face. Genesis, 49(4): 177–189
Martin P. R., Bonier F., Moore I. T., Tewksbury J. J. 2009. Latitudinal variation in the asynchrony of seasons: Implications for higher rates of population differentiation and speciation in the tropics. Ideas Ecol Evol, 2: 9–17
Myers N., Mittermeier R. A., Mittermeier C. G., Da Fonseca G. A., Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature, 403(6772): 853–858
Northcutt R. G. 2002. Understanding vertebrate brain evolution. Integr Comp Biol, 42(4): 743–756
Olori J. C. 2010. Digital endocasts of the cranial cavity and osseous labyrinth of the burrowing snake Uropeltis woodmasoni (Alethinophidia: Uropeltidae). Copeia, 2010(1): 14–26
Paluh, D. J., Stanley, E. L., Blackburn, D. C. 2020. Evolution of hyperossification expands skull diversity in frogs. Proc Natl Acad Sci USA, 117(15): 8554–8562
Pollen A. A., Dobberfuhl A. P., Scace J., Igulu M. M., Renn S. C., Shumway C. A., Hofmann H. A. 2007. Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain Behav Evol, 70(1): 21–39
Powell B. J., Leal M. 2014. Brain organization and habitat complexity in Anolis lizards. Brain Behav Evol, 84(1): 8–18
R Development Core Team. 2008. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org, 8/11/2021
Rambaut A., Drummond A. J., Xie D., Baele G., Suchard M. A. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol, 67(5): 901–904
Raveloson H., Le Minor J. M., Rumpler Y., Schmittbuhl M. 2005. Shape of the lateral mandibular outline in Lemuridae: A quantitative analysis of variability using elliptical Fourier analysis. Folia Primatol, 76(5): 245–261
Ronquist F., Teslenko M., Van Der Mark P., Ayres D. L., Darling A., H?hna S., Larget B., Liu L., Suchard M. A., Huelsenbeck J. P. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol, 61(3): 539–542
Scherle W. 1970. A simple method for volumetry of organs in quantitative stereology. Mikroskopie, 26: 57–60
Silvestro D., Michalak I. 2012. raxmlGUI: A graphical front-end for RAxML. Org Divers Evol, 12(4): 335–337
Sol D. 2009. Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol Lett, 5(1690): 130–133
Sol D., Duncan R. P., Blackburn T. M., Cassey P., Lefebvre L. 2005. Big brains, enhanced cognition, and response of birds to novel environments. Proc Natl Acad Sci USA, 102(15): 5460–5465
Sol D., Székely T., Liker A., Lefebvre L. 2007. Big-brained birds survive better in nature. Proc R Soc B Biol Sci, 274(1611): 763–769
Song Z. M., Huang D. M., Chang C. 1990. On the development and population age structure of Scutiger boulengeri tadpoles. Dongwu xuébào, 36(2): 187–193 (In Chinese)
Subba B., Ravikanth G., Aravind N. 2015. Scaling new heights: First record of Boulenger’s Lazy Toad Scutiger boulengeri (Amphibia: Anura: Megophryidae) from high altitude lake in Sikkim Himalaya, India. J Threat Taxa, 7(10): 7655–7663
Suchard M. A., Lemey P., Baele G., Ayres D. L., Drummond A. J., Rambaut A. 2018. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol, 4(1): vey016
Taylor G. M., Nol E., Boire D. 1995. Brain regions and encephalization in anurans: Adaptation or stability? Brain Behav Evol, 45(2): 96–109
Van Schaik C. P., Isler K., Burkart J. M. 2012. Explaining brain size variation: from social to cultural brain. Trends Cogn Sci, 16(5): 277–284
van Woerden J. T., van Schaik C. P., Isler K. 2010. Effects of seasonality on brain size evolution: Evidence from strepsirrhine primates. Am Nat, 176: 758–767
Vidal‐García M., Byrne P., Roberts J., Keogh J. S. 2014. The role of phylogeny and ecology in shaping morphology in 21 genera and 127 species of Australo-Papuan myobatrachid frogs. J Evol Biol, 27(1): 181–192
Wei G., Wang B., Xu N., Li Z. Z., Jiang J. P. 2009. Morphological evolution from aquatic to terrestrial in the genus Oreolalax (Amphibia, Anura, Megophryidae). Prog Nat Sci, 19(10): 1403–1408
Wen L. 2014. Uplift of the Tibetan Plateau influenced the morphological evolution of animals. J Agric Sci, 6(12): 244–250
Xin Z. 2021. Oxygen content in the atmosphere of the Tibetan Plateau (1980–2019). National Tibetan Plateau Data Center. Retrieved from https://doi.org/10.11888/Meteoro.tpdc.271156, 10/10/2021
Yang T. 2018. Molecular Phylogenetics, Biogeography and Evolution of Rhacophorus (Rhacophoridae: Amphibia). Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu. (In Chinese)
Ye C. Y., Fei L., Wei G., Xu N. 1992. Study on the phylogenetic relationship between species of Scutiger genus in Qinghai-Xizang Plateau (Amphibia: Pelobatidae). Acta Herpetol Sin, 27–39 (In Chinese)
Yu X., Zhong M. J., Li D. Y., Jin L., Liao W. B., Kotrschal A. 2018. Large-brained frogs mature later and live longer. Evolution, 72(5): 1174–1183
Zeng Y., Lou S. L., Liao W. B., Jehle R., Kotrschal A. 2016. Sexual selection impacts brain anatomy in frogs and toads. Evol Ecol, 6(19): 7070–7079


Last Update: 2022-12-25