• Jelena Krstičić Račković Faculty of Sciences, Kosovska Mitrovica
  • Nataša Tomašević Kolarov Department of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”, University of Belgrade, Bulevar Despota Stefana 142, Belgrade 11060, Serbia
  • Tanja Vukov Department of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”, University of Belgrade, Bulevar Despota Stefana 142, Belgrade 11060, Serbia
Keywords: Cranium, Sexual dimorphism, Geometric morphometrics,


Sexual size and shape dimorphism is a very common phenomenon widely studied in the field of evolutionary biology. The differences between sexes are related to their life strategies and driven by the two evolutionary processes, sexual and natural selection. In amphibians, females are larger sex due to high correlation with fecundity, while dimorphism in body shape is often related to intrasexual competition for opposite sex during the breeding season. The main aim of this study is to describe patterns of ventral cranial size and shape variation between males and females of three species of European brown frogs, Rana dalmatina, R. graeca, R. temporaria, from the Balkan Peninsula. Our results showed that species R. dalmatina and R. graeca are sexually dimorphic for the ventral cranial size while species R. graeca and R. temporaria for the ventral cranial shape. Sexual dimorphism in cranial size is most probably an indirect consequence of natural selection favoring larger body for higher fecundity in explosive breeders like brown frogs. Cranial shape variation is under a strong influence of size variation but without allometric scaling between sexes. Sexual shape differences of analyzed brown frog species were most pronounced in the level of connection between cranium and jaw which indicate that differential diet of males and females can be a factor affecting observed sexual dimorphism patterns. More detailed studies of males and females microhabitats are necessary to conclude if differences in intersexual ecology affect intersexual size and shape differences in the cranium.


Andersson, M. B. 1994. Sexual selection. Princeton, New Jersey: Princeton University Press.

Bell, R. C., & Zamudio, K. R. 2012. Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity. Proceedings of the Royal Society B: Biological Sciences, 279, pp. 4687-4693. doi: 10.1098/rspb.2012.1609

Berns, C. M. 2013. The evolution of sexual dimorphism: understanding mechanisms of sexual shape differences, Sexual Dimorphism, IntechOpen doi:10.5772/55154

Bonduriansky, R. 2006. Convergent evolution of sexual shape dimorphism in Diptera. Journal of Morphology, 267(5), pp. 602-611. doi:10.1002/jmor.10426

Borczyk, B., Kusznierz, J., Paśko, Ł., & Turniak, E. 2014. Scaling of the sexual size and shape skull dimorphism in the sand lizard (Lacerta agilis L.). Vertebrate Zoology, 64(2), pp. 221-227.

Cardini, A., & Elton, S. 2007. Sample size and sampling error in geometric morphometric studies of size and shape. Zoomorphology, 126(2), pp. 121-134. doi:10.1007/s00435-007-0036-2

Cicort-Lucaciu, A. S., Sas, I., Roxin, M., Badar, L., & Goilean, C. 2011. The feeding study of a Rana dalmatina population from Carei Plain, South Western Horticulture. Biology and Environment, 2(1), pp. 35-46.

Cooper, M. I. 2018. Sexual size dimorphism and the rejection of Rensch’s rule in Diplopoda (Arthropoda). Journal of Entomology and Zoology Studies, 6(1v), pp. 1582-1587. doi:10.22271/j.ento.2018.v6.i1v.07

Cox, R. M., & Calsbeek, R. 2010. Sex‐specific selection and intraspecific variation in sexual size dimorphism. Evolution: International Journal of Organic Evolution, 64(3), pp. 798-809. doi: 10.1111/j.1558-5646.2009.00851.x

Dryden, I. L., & Mardia, K.V. 1998. Statistical analysis of shape. New York: John Wiley and Sons.

Džukić, G., & Kalezić, M. L. 2004. The biodiversity of amphibians and reptiles in the Balkan Peninsula. In H.I. Griffiths, B. Kryštufek, & J.M. Reed Eds., Balkan biodiversity: Pattern and process in the European hotspot.Dordrecht: Springer Nature. pp. 167-192; doi: 10.1007/978-1-4020-2854-0_10

Džukić, G., Cvijanović, M., Urošević, A., Vukov, T. D., Tomašević Kolarov, N., Slijepčević, M., Ivanović, A., & Kalezić, M. L. 2015. The batrachological collections of the Institute for biological research "Siniša Stanković", University of Belgrade. Bulletin of the Natural History Museum in Belgrade, 8, pp. 118-167. doi:10.5937/bnhmb1508118D

Fairbairn, D. J. 1997. Allometry for sexual size dimorphism: Pattern and Process in the Coevolution of Body Size in Males and Females. Annual Review of Ecology and Systematics, 28(1), pp. 659-687. doi:10.1146/annurev.ecolsys.28.1.659

Fairbairn, D. J. 2013. Odd Couples: Extraordinary differences between the sexes in the animal kingdom. Princeton: Walter de Gruyter GmbH. doi:10.1515/9781400847600

Fairbairn, D. J., Blanckenhorn, W.U., Székely, T., & Eds., 2007. Sex, size and gender roles: Evolutionary studies of sexual size dimorphism. Oxford: Oxford University Press. doi: 10.1093/acprof: oso/9780199208784.001.0001

Friedman, N. R., & Remeš, V. 2016. Global geographic patterns of sexual size dimorphism in birds,port for a latitudinal trend. Ecography, 39(1), pp. 17-25. sup; doi: 10.1111/ecog.01531

Gittleman, J. L., & Van, V. B. 1997. Sexual dimorphism in the canines and skulls of carnivores: effects of size, phylogency, and behavioural ecology. Journal of Zoology, 242(1), pp. 97-117. doi: 10.1111/j.1469-7998.1997.tb02932.x

Hallgrímsson, B., & Hall, B. K. 2005. Variation and variability: Central concepts in biology. In B. Hallgrímsson & B. K. Hall Eds., Variation. Burlington, MA, USA: Elsevier. pp. 1-7; doi: 10.1016/B978-012088777-4/50003-X

Hendry, C. R., Guiher, T. J., & Pyron, R. A. 2014. Ecological divergence and sexual selection drive sexual size dimorphism in new world pitvipers (Serpentes: Viperidae). Journal of evolutionary biology, 27(4), pp. 760-771. doi: 10.1111/jeb.12349

Herrel, A., Damme, R. V., Vanhooydonck, B., & Vree, F. D. 2001. The implications of bite performance for diet in two species of lacertid lizards. Canadian Journal of Zoology, 79, pp. 662-670. doi: 10.1139/z01-031

Herrel, A., Mcbrayer, L., & Larson, P. 2007. Functional basis for sexual differences in bite force in the lizard Anolis carolinensis. Biological Journal of the Linnean Society, 91, pp. 111-119. doi: 10.1111/j.1095-8312.2007.00772.x

Herrel, A., Spithoven, L., van Damme, R., & Vree, F. D. 1999. Sexual dimorphism of head size in Gallotia galloti: testing the niche divergence hypothesis by functional analyses. Functional Ecology, 13(3), pp. 289-297. doi: 10.1046/j.1365-2435.1999.00305.x

Hoffman, E. A., & Blouin, M. S. 2000. A review of colour and pattern polymorphisms in anurans. Biological Journal of the Linnean Society, 70(4), pp. 633-665. doi: 10.1111/j.1095-8312.2000.tb00221.x

Ivanović, A., & Kalezić, M. L. 2012. Sexual dimorphism in the skull geometry of newt species of Ichthyosaura, Triturus and Lissotriton (Salamandridae, Caudata Amphibia). Zoomorphology, 131(1), pp. 69-78. doi: 10.1007/s00435-011-0143-y

Ivanović, A., Sotiropoulos, K., Furtula, M., Džukić, G., & Kalezić, M. L. 2008. Sexual size and shape evolution in European newts (Amphibia: Caudata: Salamandridae) on the Balkan Peninsula. Journal of Zoological Systematics and Evolutionary Research, 46(4), pp. 381-387. doi: 10.1111/j.1439-0469.2008.00479.x

Ivanović, A., Vukov, T. D., Džukić, G., Tomašević, N., & Kalezić, M. L. 2007. Ontogeny of skull size and shape changes within a framework of biphasic lifestyle: a case study in six Triturus species (Amphibia, Salamandridae). Zoomorphology, 126(3), pp. 173-183. doi: 10.1007/s00435-007-0037-1

Kaliontzopoulou, A., Carretero, M. A., & Llorente, G. A. 2007. Multivariate and geometric morphometrics in the analysis of sexual dimorphism variation in Podarcis lizards. Journal of Morphology, 268, pp. 152-165. doi: 10.1002/jmor.10494

Klingenberg, C. P. 2010. MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), pp. 353-357. doi:10.1111/j.1755-0998.2010.02924.x

Krstičić, R. J., Tomašević, K. N. T., Labus, N., & Vukov, T. 2019. Interspecific size-and sex-related variation in the cranium of European brown frogs (Genus Rana). Zoomorphology, 138(2), pp 277–286. doi: 10.1007/s00435-019-00441-9

Kuo, C. Y., Lin, Y. T., & Lin, Y. S. 2009. Sexual size and shape dimorphism in an Agamid lizard, Japalura swinhonis (Squamata: Lacertilia: Agamidae). Zoological Studies, 48(3), pp. 351-361.

Lailvaux, S. P., Huyghe, K., & Van, D. R. 2012. 'Why can't we all just get along?, Interspecific aggression in resident and non‐resident Podarcis melisellensis lizards'. Journal of Zoology, 288(3), pp. 207-213. doi: 10.1111/j.1469-7998.2012.00943.x

Lappin, A. K., & Husak, J. F. 2005. Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris). The American Naturalist, 166(3), pp. 426-436. doi: 10.1086/432564

Ljubisavljević, K., Urošević, A., Aleksić, I., & Ivanović, A. 2010. Sexual dimorphism of skull shape in a lacertid lizard species (Podarcis spp. Dalmatolacerta sp. Dinarolacerta sp.) revealed by geometric morphometrics. Zoology, 113(3), pp. 168-174. doi: 10.1016/j.zool.2009.09.003

Mcbrayer, L. D., & Anderson, R. A. 2007. Sexual size dimorphisms and bite force in the northern alligator lizard, Elgaria coerulea. Journal of Herpetology, 41(4), pp. 554-560. doi: 10.1670/07-045.1

Mcpherson, F. J., & Chenoweth, P. J. 2012. Mammalian sexual dimorphism. Animal reproduction science, 131(3-4), pp. 109-122. doi: 10.1016/j.anireprosci.2012.02.007

Monnet, J. M., & Cherry, M. I. 2002. 'Sexual size dimorphism in anurans', Proceedings of the Royal Society of London. Series B: Biological Sciences, 269(1507), pp. 2301-2307. doi: 10.1098/rspb.2002.2170

Morris, J. S., & Carrier, D. R. 2016. Sexual selection on skeletal shape in Carnivora. Evolution, 70(4), pp. 767-780. doi: 10.1111/evo.12904

Ng, T. P., Rolán-Alvarez, E., Dahlén, S. S., Davies, M. S., Estévez, D., Stafford, R., & Williams, G. A. 2019. The causal relationship between sexual selection and sexual size dimorphism in marine gastropods. Animal Behaviour, 148, pp. 53-62. doi: 10.1016/j.anbehav.2018.12.005

Peiman, K., & Robinson, B. 2010. Ecology and evolution of resource-related heterospecific aggression. The Quarterly Review of Biology, 85(2), pp. 133-158. doi: 10.1086/652374

Petrović, T. G., Vukov, T. D., & Kolarov, N. T. 2017. Sexual dimorphism in size and shape of traits related to locomotion in nine anuran species from Serbia and Montenegro. Folia Zoologica, 66(1), pp. 11-22. doi: 10.25225/fozo.v66.i1.a4.2017

Plavcan, J. M. 2012. Sexual Size Dimorphism, Canine Dimorphism, and Male-Male Competition in Primates. Human Nature, 23(1), pp. 45-67. doi:10.1007/s12110-012-9130-3

Porobić, J., Ćirović, D., & Jojić, V. 2016. Cranial variability of the Serbian golden jackal: Geographic variation, sexual dimorphism and allometry. Zoologischer Anzeiger-A Journal of Comparative Zoology, 261, pp. 38-47. doi: 10.1016/j.jcz.2016.03.004

Price, T. D. 1984. The Evolution of Sexual Size Dimorphism in Darwin's Finches. The American Naturalist, 123(4), pp. 500-518. doi:10.1086/284219

R Core Team 2015. R: a language and environment for statistical computing, Version 3.2.0, R Foundation for Statistical Computing, Vienna,

Rohlf, F. J. 2008. TpsDig. In Ecology and Evolution. SUNY at Stony Brook. Version 2.12.

Sacchi, R., Pupin, F., Gentilli, A., Rubolini, D., Scali, S., Fasola, M., & Galeotti, P. 2009. Male-male combats in a polymorphic lizard: Residency and size, but not color, affect fighting rules and contest outcome, Aggressive Behavior. Official Journal of the International Society for Research on Aggression, 35(3), pp. 274-283. doi: 10.1002/ab.20305

Shine, R. 1979. Sexual Selection and Sexual Dimorphism in the Amphibia. Copeia, 1979(2), p. 297. doi:10.2307/1443418

Shine, R. 1989. Ecological Causes for the Evolution of Sexual Dimorphism: A Review of the Evidence. The Quarterly Review of Biology, 64(4), pp. 419-461. doi:10.1086/416458

Sillero, N., Campos, J., Bonardi, A., Corti, C., Creemers, R., Crochet, P. A., Crnobrnja Isailović, J., Denoël, M., Ficetola, G. F., Gonçalves, J., Kuzmin, S., Lymberakis, P., de Pous, P., Rodríguez, A., Sindaco, R., Speybroeck, J., Toxopeus, B., Vieites, D. R., Vences, M. 2014. Updated distribution and biogeography of amphibians and reptiles of Europe. Amphibia-Reptilia, 35(1), pp. 1-31. doi:10.1163/15685381-00002935

Snyder, N. F., & Wiley, J. W. 1976. Sexual size dimorphism in hawks and owls of North America. Ornithological Monograph. Washington DC: American Ornithologists' Union. no. 20; doi: 10.2307/40166710

-StatSoft, Inc. 2011. Statistica (data analysis software system). version 10,

Vincent, S.E., Herrel, A., & Irschick, D.J. 2004. Sexual dimorphism in head shape and diet in the cottonmouth snake (Agkistrodon piscivorus). Journal of Zoology, 264(1), pp. 53-59. doi: 10.1017/S0952836904005503

Vladić, Ž. J., Benítez, H. A., Pirnat, A., Hristovski, S., & Jelaska, L. Š. 2019. Variations in body shape of mountain habitat specialist Carabus croaticus and its sister species Carabus caelatus (Coleoptera: Carabidae) populations across Dinaric Alps. Zoomorphology, 138(1), pp. 85-96. doi: 10.1007/s00435-018-0428-5

Vukov, T., Krstičić, J., Petrović, T., & Tomašević, K. N. 2018. Patterns of cranial sexual dimorphism in the yellow-bellied toad (Bombina variegata, Bombinatoridae). North-Western Journal of Zoology, 14(1), pp. 44-49.

Woolbright, L. L. 1983. Sexual Selection and Size Dimorphism in Anuran Amphibia. The American Naturalist, 121(1), pp. 110-119. doi:10.1086/284042

Zhang, L., & Lu, X. 2013. Sexual size dimorphism in anurans: ontogenetic determination revealed by an across-species comparison. Evolutionary Biology, 40(1), pp. 84-91. doi: 10.1007/s11692-012-9187-2

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