Abstract
The vertebrate skull is considered as phylogenetically conserved, but shows extensive diversification in many clades due to various environmental, climate and habitat influences. We explored the cranial size and shape differences of three closely related brown frog species, Rana temporaria, R. dalmatina and R. graeca to emphases the interspecific variation and intraspecific sexual differences, the allometric patterns in cranial shape changes and the relationship between cranial shape, phylogeny, and ecological similarity. Brown frogs significantly differ in cranial size and shape. Interspecific cranial shape changes are under strong influence of size variation. When size is considered, our results show that R. dalmatina is the most divergent species, while differences between R. dalmatina and R. temporaria cranial shapes are diminished when size is removed and peculiar features of R. graeca cranium arise (the most robust and rounded cranium). In both cases, with size and without size, major shape changes are related to the position of quadratum and width of the cranium at the level of anterior margin of eye. When comparing non-allometric shape with ecological similarity and phylogenetic relatedness we found that ecologically similar but phylogenetically more distant species shared the cranial morphology. Intraspecific patterns of cranial phenotypic variation in brown frogs showed significant cranium sexual size and shape dimorphism and absence of allometric scaling between sexes. More detailed studies on the relation of morphology and ecology in brown frogs are necessary to explain the mechanism behind cranial size and shape variation.
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References
Arroyo SB, Serrano-Cardozo VH, Ramirez-Pinilla MP (2008) Diet, microhabitat and time of activity in a Pristimantis (Anura, Strabomantidae) assemblage. Phyllomedusa 7:109–119. https://doi.org/10.11606/issn.2316-9079.v7i2p109–119
Aszalós L, Bogdan H, Kovács ÉH, Peter VI (2005) Food composition of two Rana species on a forest habitat (Livada Plain, Romania). Northwest J Zool 1:25–30
Atchley WR, Rutledge JJ, Cowley DE (1981) Genetic components of size and shape. II. Multivariate covariance patterns in the rat and mouse skull. Evolution 35:1037–1055. https://doi.org/10.1111/j.1558-5646.1981.tb04973.x
Bennett CV, Goswami A (2013) Statistical support for the hypothesis of developmental constraint in marsupial skull evolution. BMC Biol 11:52. https://doi.org/10.1186/1741-7007-11-52
Bisa R, Sfenthourakis S, Fraguedakis-Tsolis S, Chondropoulos B (2007) Population density and food analysis of Bombina variegata and Rana graeca in mountainous riverine ecosystems of northern Pindos (Greece). J Biol Res Thessalon 8:129–137
Bull CM, Pamula Y (1996) Sexually dimorphic head sizes and reproductive success in the sleepy lizard Tiliqua rugosa. J Zool 240:511–521. https://doi.org/10.1111/j.1469-7998.1996.tb05302.x
Burress ED (2015) Cichlid fishes as models of ecological diversification: patterns, mechanisms, and consequences. Hydrobiologia 748:7–27. https://doi.org/10.1007/s10750-014-1960-z
Cardini A, Elton S (2007) Sample size and sampling error in geometric morphometric studies of size and shape. Zoomorphology 126:121–134. https://doi.org/10.1007/s00435-007-0036-2
Caumul R, Polly PD (2005) Phylogenetic and environmental components of morphological variation: skull, mandible, and molar shape in marmots (Marmota Rodentia) Evolution 59:2460–2472. https://doi.org/10.1111/j.0014-3820.2005.tb00955.x
Çiçek K, Mermer A (2007) Food composition of the marsh frog, Rana ridibunda Pallas, 1771, in Thrace. Turk J Zool 31:83–90
Cicort-Lucaciu AS, Sas I, Roxin M, Badar L, Goilean C (2011) The feeding study of a Rana dalmatina population from Carei Plain. South West J Hortic Biol Environ 2:35–46
Claude J, Pritchard P, Tong H, Paradis E, Auffray J-C (2004) Ecological correlates and evolutionary divergence in the skull of turtles: a geometric morphometric assessment. Syst Biol 53:933–948. https://doi.org/10.1080/10635150490889498
Derryberry EP, Claramunt S, Derryberry G, Chesser RT, Cracraft J, Aleixo A, Pérez-Emán J, Remsen JV, Brumfield RT (2011) Lineage diversification and morphological evolution in a large-scale continental radiation: the Neotropical ovenbirds and woodcreepers (Aves: Furnariidae). Evolution 65:2973–2986. https://doi.org/10.1111/j.1558-5646.2011.01374.x
Dimancea N, Covaciu-Marcov SD (2009) The trophic spectrum of a Bufo bufo population (Amphibia) from Iezer Mountain, Arge County, Romania. An Univ Craiova Ser biol 14:469–474
Dollion AY, Measey GJ, Cornette R, Carne L, Tolley KA, da Silva JM, Boistel R, Fabre AC, Herrel A (2017) Does diet drive the evolution of head shape and bite force in chameleons of the genus Bradypodion? Funct Ecol 31:671–684. https://doi.org/10.1111/1365-2435.12750
Dryden IL, Mardia KV (1998) Statistical analysis of shape. Wiley, New York
Džukić G, Kalezić ML (2004) The biodiversity of amphibians and reptiles in the Balkan Peninsula. In: Griffiths HI, Kryštufek B, Reed JM (eds) Balkan biodiversity. Springer, Dordrecht, pp 167–192
Džukić G, Cvijanović M, Urošević A, Vukov TD, Tomašević-Kolarov N, Slijepčević M, Ivanović A, Kalezić ML (2015) The batrachological collections of the Institute for biological research “Siniša Stanković”, University of Belgrade. Bull Mus Nat Hist Belgrade 8:118–167. https://doi.org/10.5937/bnhmb1508118D
Emerson SB (1985) Skull shape in frogs: correlations with diet. Herpetologica 1985:177–188
Emerson SB, Voris H (1992) Competing explanations for sexual dimorphism in a voiceless Bornean frog. Funct Ecol 6:654–660. https://doi.org/10.2307/2389960
Emerson SB, Greene HW, Charnov EL (1994) Allometric aspects of predator-prey interactions. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. Chicago University Press, Chicago, pp 123–139
Fabre AC, Bickford D, Segall M, Herrel A (2016) The impact of diet, habitat use, and behaviour on head shape evolution in homalopsid snakes. Biol J Linn Soc 118:634–647. https://doi.org/10.1111/bij.12753
Foote M (1997) The evolution of morphological diversity. Annu Rev Ecol Syst 28:129–152. https://doi.org/10.1146/annurev.ecolsys.28.1.129
Gollmann G, Baumgartner C, Gollmann B, Waringer-Löschenkohl A (1999) Breeding phenology of syntopic frog populations, Rana dalmatina and Rana temporaria, in suburban Vienna. Ver Gesell Okologie 29:357–362
Hall BK (2008) Fins into limbs: evolution, development, and transformation. Chicago University Press, Chicago
Hall BK (2012) Evolutionary developmental biology. Springer, New York
Hallgrímsson B, Hall BK (2005) Variation: a central concepts in biology. Academic Press, New York
Hanken J, Gross JB (2005) Evolution of cranial development and the role of neural crest: insights from amphibians. J Anat 207:437–446. https://doi.org/10.1111/j.1469-7580.2005.00481.x
Hanken J, Hall BK (1988) Skull development during anuran metamorphosis. II. Role of thyroid hormone in osteogenesis. Anat Embryol 178:219–227. https://doi.org/10.1007/BF00318225
Hanken J, Hall BK (1993) Mechanisms of skull diversity and evolution. In: Hanken J, Hall BK (eds) The skull volume 3. Chicago University Press, Chicago, pp 1–36
Hanken J, Summers CH (1988) Skull development during anuran metamorphosis: III. Role of thyroid hormone in chondrogenesis. J Exp Zool 246:156–170. https://doi.org/10.1002/jez.1402460208
Hanken J, Thorogood P (1993) Evolution and development of the vertebrate skull: the role of pattern formation. Trends Ecol Evol 8:9–15. https://doi.org/10.1016/0169-5347(93)90124-8
Herrel A, de Grauw E, Lemos-Espinal JA (2001) Head shape and bite performance in xenosaurid lizards. J Exp Zool 290:101–107. https://doi.org/10.1002/jez.1039
Herrel A, McBrayer LD, Larson PM (2007) Functional basis for sexual differences in bite force in the lizard Anolis carolinensis. Biol J Linn Soc 91:111–119. https://doi.org/10.1111/j.1095-8312.2007.00772.x
Herrel A, Podos J, Vanhooydonck B, Hendry AP (2009) Force-velocity trade-off in Darwin’s finch jaw function: a biomechanical basis for ecological speciation? Funct Ecol 23:119–125. https://doi.org/10.1111/j.1365-2435.2008.01494.x
Herrel A, Petrochic S, Draud M (2018) Sexual dimorphism, bite force and diet in the diamondback terrapin. J Zool 304:217–224. https://doi.org/10.1111/jzo.12520
Hodisan OI, Benchiş A, Gabrian D, Badar L, Toader S (2010) The trophic spectrum of two brown frog populations (Rana dalmatina and Rana temporaria) from Baia de Fier area, Romania. Herpetol Rom 4:7–16
Hood GM (2010) PopTools, version 3.2.5. http://www.poptools.org
Ivanović A, Arntzen JW (2014) Evolution of skull and body shape in Triturus newts reconstructed from three-dimensional morphometric data and phylogeny. Biol J Linn Soc 113:243–255. https://doi.org/10.1111/bij.12314
Ivanović A, Arntzen JW (2018) Evolution of skull shape in the family Salamandridae (Amphibia: Caudata). J Anat 232:359–370. https://doi.org/10.1111/joa.12759
Ivanović A, Vukov TD, Džukić G, Tomašević Kolarov N, Kalezić ML (2007) Ontogeny of skull size and shape changes within a framework of biphasic lifestyle: a case study in six Triturus species (Amphibia, Salamandridae). Zoomorphology 126:173–183. https://doi.org/10.1007/s00435-007-0037-1
Kaliontzopoulou A, Carretero MA, Llorente GA (2007) Head shape allometry and proximate causes of head sexual dimorphism in Podarcis lizards: joining linear and geometric morphometrics. Biol J Linn Soc 93:111–124. https://doi.org/10.1111/j.1095-8312.2007.00921.x
Kaliontzopoulou A, Carretero MA, Llorente GA (2010) Intraspecific ecomorphological variation: linear and geometric morphometrics reveal habitat-related patterns within Podarcis bocagei wall lizards. J Evol Biol 23:1234–1244. https://doi.org/10.1111/j.1420-9101.2010.01984.x
Kaliontzopoulou A, Adams DC, van der Meijden A, Perera A, Carretero M (2012) Relationships between head morphology, bite performance and ecology in two species of Podarcis wall lizards. Evol Ecol 26:825–845. https://doi.org/10.1007/s10682-011-9538-y
Katsikaros K, Shine R (1997) Sexual dimorphism in the tusked frog, Adelotus brevis (Anura: Myobatrachidae): the roles of natural and sexual selection. Biol J Linn Soc 60:39–51
Klaczko J, Sherratt E, Setz EZ (2016) Are diet preferences associated to skulls shape diversification in xenodontine snakes? PLoS One 11:e0148375. https://doi.org/10.1371/journal.pone.0148375
Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
Kohlsdorf T, Grizante MB, Navas CA, Herrel A (2008) Head shape evolution in Tropidurinae lizards: does locomotion constrain diet? J Evol Biol 21:781–790. https://doi.org/10.1111/j.1420-9101.2008.01516.x
Kovács I, David A, Ferenţi S, Dimancea N (2010) The food composition of two brown frog populations (Rana dalmatina and Rana temporaria) from Sălaj County, Romania. Bih Biol 4:7–14
Kupfer A (2007) Sexual size dimorphism in amphibians: an overview. In: Fairbairn DJ, Blanckenhorn WU, Szekely T (eds) Sex, size and gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, Oxford, pp 50–60
Lappin AK, Wilcox SC, Moriarty DJ, Stoeppler SA, Evans SE, Jones ME (2017) Bite force in the horned frog (Ceratophrys cranwelli) with implications for extinct giant frogs. Sci Rep UK 7:11963. https://doi.org/10.1038/s41598-017-11968-6
Lima AP, Magnusson WE (1998) Partitioning seasonal time interactions among size, foraging activity and diet in leaf-litter frogs. Oecologia 116:259–266. https://doi.org/10.1007/s004420050587
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 113:168–174. https://doi.org/10.1016/j.zool.2009.09.003
Maestri R, Patterson BD, Fornel R, Monteiro LR, De Freitas TRO (2016) Diet, bite force and skull morphology in the generalist rodent morphotype. J Evol Biol 29:2191–2204. https://doi.org/10.1111/jeb.12937
Marroig G, Cheverud JM (2001) A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of New World monkeys. Evolution 55:2576–2600. https://doi.org/10.1111/j.0014-3820.2001.tb00770.x
Marroig G, Cheverud JM (2004) Did natural selection or genetic drift produce the cranial diversification of neotropical monkeys? Am Nat 163:417–428. https://doi.org/10.1086/381693
Martínez-Abadías N, Esparza M, Sjøvold T, González-José R, Santos M, Hernández M, Klingenberg CP (2012) Pervasive genetic integration directs the evolution of human skull shape. Evolution 66:1010–1023. https://doi.org/10.1111/j.1558-5646.2011.01496.x
McCurry MR, Evans AR, Fitzgerald EM, Adams JW, Clausen PD, McHenry CR (2017a) The remarkable convergence of skull shape in crocodilians and toothed whales. Proc R Soc B 284:20162348. https://doi.org/10.1098/rspb.2016.2348
McCurry MR, Fitzgerald EM, Evans AR, Adams JW, McHenry CR (2017b) Skull shape reflects prey size niche in toothed whales. Biol J Linn Soc 121:936–946. https://doi.org/10.1093/biolinnean/blx032
Nali RC, Zamudio KR, Haddad CF, Prado CP (2014) Size-dependent selective mechanisms on males and females and the evolution of sexual size dimorphism in frogs. Am Nat 184:727–740. https://doi.org/10.1086/678455
Ollonen J, Da Silva FO, Mahlow K, Di-Poï N (2018) Skull development, ossification pattern, and adult shape in the emerging lizard model organism Pogona vitticeps: a comparative analysis with other squamates. Front Physiol 9:278. https://doi.org/10.3389/fphys.2018.00278
Olsson M, Shine R, Wapstra E, Ujvari B, Madsen T (2002) Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection. Evolution 56:1538–1542. https://doi.org/10.1111/j.0014-3820.2002.tb01464.x
Ospina-Garcés SM, De Luna E, Herrera M, Gerardo L, Flores-Martínez JJ (2016) Cranial shape and diet variation in Myotis species (Chiroptera: Vespertilionidae): testing the relationship between form and function. Acta Chiropterol 18:163–180. https://doi.org/10.3161/15081109ACC2016.18.1.007
Perkins MW, Eason PK (2018) The relationship of head morphology and diet among three sympatric watersnake species. Amphibia Reptilia. https://doi.org/10.1163/15685381-20181042
Ponssa ML, Candioti MFV (2012) Patterns of skull development in anurans: size and shape relationship during postmetamorphic cranial ontogeny in five species of the Leptodactylus fuscus Group (Anura: Leptodactylidae). Zoomorphology 131:349–362. https://doi.org/10.1007/s00435-012-0164-1
Porto A, de Oliveira FB, Shirai LT, De Conto V, Marroig G (2009) The evolution of modularity in the mammalian skull I: morphological integration patterns and magnitudes. Evol Biol 36:118–135. https://doi.org/10.1007/s11692-008-9038-3
Preest MR (1994) Sexual size dimorphism and feeding energetics in Anolis carolinensis: why do females take smaller prey than males? J Herpetol 28:292–298. https://doi.org/10.2307/1564527
Pyron RA, Wiens JJ (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phylogenet Evol 61:543–583. https://doi.org/10.1016/j.ympev.2011.06.012
R Core Team (2017) R: a language and environment for statistical computing (Version 3.4.2). R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ricklefs RE, Miles DB (1994) Ecological and evolutionary inferences from morphology: an ecological perspective. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. Chicago University Press, Chicago, pp 13–41
Riis N (1991) A field study of survival, growth, biomass and temperature dependence of Rana dalmatina and Rana temporaria larvae. Amphibia Reptilia 12:229–243. https://doi.org/10.1163/156853891X00419
Rocek Z, Rage JC (2000) Anatomical transformations in the transition from temnospondyl to proanuran stages. Amphib Biol 4:1274–1282
Rohlf FJ (2008) TpsDig. Version 2.12. Ecology and Evolution, SUNY at Stony Brook
Rose CS, Reiss JO (1993) Metamorphosis and the vertebrate skull: ontogenetic patterns and developmental mechanisms. In: Hanken J, Hall BK (eds) The skull, vol 1. Chicago University Press, Chicago, pp 289–346
Runemark A, Sagonas K, Svensson EI (2015) Ecological explanations to island gigantism: dietary niche divergence, predation, and size in an endemic lizard. Ecology 96:2077–2092. https://doi.org/10.1890/14-1996.1
Santana SE, Grosse IR, Dumont ER (2012) Dietary hardness, loading behavior, and the evolution of skull form in bats. Evolution 66:2587–2598. https://doi.org/10.1111/j.1558-5646.2012.01615.x
Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, New York
Schoch RR (2014) Amphibian skull evolution: the developmental and functional context of simplification, bone loss and heterotopy. J Exp Zool Part B 322:619–630. https://doi.org/10.1002/jez.b.22599
Schoenebeck JJ, Ostrander EA (2013) The genetics of canine skull shape variation. Genetics 193:317–325. https://doi.org/10.1534/genetics.112.145284
Sheil CA, Jorgensen M, Tulenko F, Harrington S (2014) Variation in timing of ossification affects inferred heterochrony of cranial bones in Lissamphibia. Evol Dev 16:292–305. https://doi.org/10.1111/ede.12092
Shine R (1979) Sexual selection and sexual dimorphism in the Amphibia. Copeia 297–306. https://doi.org/10.2307/1443418
Shubin NH, Jenkins FA (1995) An early Jurassic jumping frog. Nature 377:49–52. https://doi.org/10.1038/377049a0
Sidlauskas B (2008) Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach. Evolution 62:3135–3156. https://doi.org/10.1111/j.1558-5646.2008.00519.x
Sigurdsen T, Bolt JR (2010) The lower Permian amphibamid Doleserpeton (Temnospondyli: Dissorophoidea), the interrelationships of amphibamids, and the origin of modern amphibians. J Vertebr Paleontol 30:1360–1377. https://doi.org/10.1080/02724634.2010.501445
Sillero N, Campos J, Bonardi A, Corti C, Creemers R, Crochet P-A, Crnobrnja Isailovic J, Denoël M, Ficetola GF, Gonçalves J, Kuzmin S, Lymberakis P, de Pous P, Rodríguez A, Sindaco R, Speybroeck J, Toxopeus B, Vieites DR, Vences M (2014) Updated distribution and biogeography of amphibians and reptiles of Europe. Amphibia Reptilia 35:1–31. https://doi.org/10.1163/15685381-00002935
Simon MN, Marroig G (2017) Evolution of a complex phenotype with biphasic ontogeny: contribution of development versus function and climatic variation to skull modularity in toads. Ecol Evol 7:10752–10769. https://doi.org/10.1002/ece3.3592
Simon MN, Machado FA, Marroig G (2016) High evolutionary constraints limited adaptive responses to past climate changes in toad skulls. Proc R Soc B 283:20161783. https://doi.org/10.1098/rspb.2016.1783
Stange M, Aguirre-Fernández G, Salzburger W, Sánchez-Villagra MR (2018) Study of morphological variation of northern Neotropical Ariidae reveals conservatism despite macrohabitat transitions. BMC Evol Biol 18:38. https://doi.org/10.1186/s12862-018-1152-y
Timm-Davis LL, DeWitt TJ, Marshall CD (2015) Divergent skull morphology supports two trophic specializations in otters (Lutrinae). PLoS One 10:e0143236. https://doi.org/10.1371/journal.pone.0143236
Trochet A, Moulherat S, Calvez O, Stevens VM, Clobert J. Schmeller DS (2014) A database of life-history traits of European amphibians. Biodivers Data J 2:e4123. https://doi.org/10.3897/BDJ.2.e4123
Üzüm N, Ivanović A, Gümüş Ç, Avcı A, Olgun K (2015) Divergence in size, but not in shape: variation in skull size and shape within Ommatotriton newts. Acta Zool-Stockholm 96:478–486. https://doi.org/10.1111/azo.12092
Veith M, Kosuch J, Vences M (2003) Climatic oscillations triggered post-Messinian speciation of Western Palearctic brown frogs (Amphibia, Ranidae). Mol Phylogenet Evol 26:310–327. https://doi.org/10.1016/S1055-7903(02)00324-X
Verwaijen D, Van Damme R, Herrel A (2002) Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards. Funct Ecol 16:842–850. https://doi.org/10.1046/j.1365-2435.2002.00696.x
Vidal-García M, Keogh JS (2017) Phylogenetic conservatism in skulls and evolutionary lability in limbs-morphological evolution across an ancient frog radiation is shaped by diet, locomotion and burrowing. BMC Evol Biol 17:165. https://doi.org/10.1186/s12862-017-0993-0
Vukov T, Kuručki M, Anđelković M, Tomašević Kolarov N (2018) Post-metamorphic ontogenetic changes in head size and shape of the pool frog (Pelophylax lessonae, Ranidae). Arch Biol Sci 70:307–312. https://doi.org/10.2298/ABS171004047V
Wainwright PC (1994) Functional morphology as a tool in ecological research. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. Chicago University Press, Chicago, pp 42–59
Woolbright LL (1983) Sexual selection and size dimorphism in anuran amphibia. Amer Nat 121:110–119. https://doi.org/10.1086/284042
Young NM, Hallgrímsson B (2005) Serial homology and the evolution of mammalian limb covariation structure. Evolution 59:2691–2704. https://doi.org/10.1111/j.0014-3820.2005.tb00980.x
Zelditch ML, Lundrigan BL, Garland T Jr (2004) Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evol Dev 6:194–206. https://doi.org/10.1111/j.1525-142X.2004.04025.x
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This study was supported by the Serbian Ministry of Education, Science and Technological Development under project No. 173043.
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TV and NTK conceived and designed study. JKR performed laboratory work. JKR, NTK, NL and TV wrote the manuscript together.
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Krstičić Račković, J., Tomašević Kolarov, N., Labus, N. et al. Interspecific size- and sex-related variation in the cranium of European brown frogs (Genus Rana). Zoomorphology 138, 277–286 (2019). https://doi.org/10.1007/s00435-019-00441-9
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DOI: https://doi.org/10.1007/s00435-019-00441-9