[en] Body size is influenced by the interaction of multiple forces, whose effects can determine the occurrence of sexual size dimorphism (SSD). Rensch's rule is the increase of SSD with body size in taxa where males are the largest sex, and the opposite pattern in female-biased SSD taxa. This pattern was detected in many animal groups, but contrasting results were also highlighted. This study evaluated the existence of Rensch's patterns for body size and for the number of caudal vertebrae in salamandrid caudate amphibians. Furthermore, we tested the support of alternative hypotheses on processes that may determine allometric patterns: sexual selection, fecundity selection and constraining selection by performing separate analyses on species with male- and female-biased SSD. We used the literature and original data to gather information on body size and number of caudal vertebrae in 52 species of salamandrids over four continents. We then tested the support of the three hypotheses using a phylogenetic approach. Rensch's rule was valid for body size in salamanders only for species with male-biased dimorphism. No allometric relationships were detected by analyses on all the species, or by analyses on female-biased SSD species. Analyses performed on the number of caudal vertebrae showed no significant patterns. Our study supports the role of sexual selection in promoting positive allometry for body size in male-biased SSD species, whereas the alternative hypotheses were not supported by our data. These results highlight the importance of distinguishing male- and female-biased species as different evolutionary pressures and constraints may be at the basis of evolution of SSD in these groups.
Research Center/Unit :
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Disciplines :
Zoology
Author, co-author :
Colleoni, E.; Università degli Studi di Milano-Bicocca, Italy
Denoël, Mathieu ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Padoa-Schioppa, E.; Università degli Studi di Milano-Bicocca, Italy
Scali, S.; Museo di Storia Naturale di Milano, Italy
Ficetola, G.F.
Language :
English
Title :
Rensch’s rule and sexual dimorphism in salamanders: patterns and potential processes
Abouheif, E. & Fairbairn, D.J. (1997). A comparative analysis of allometry for sexual size dimorphism: assessing Rensch's rule. Am. Nat. 149, 540-562.
AmphibiaWeb (2014). Information on amphibian biology and conservation. [web application]. Berkeley, CA: AmphibiaWeb. URL http://amphibiaweb.org/ [accessed 20 February 2014].
Blanckenhorn, W.U., Dixon, A.F.G., Fairbairn, D.J., Foellmer, M.W., Gibert, P., Van Der Linde, K., Meier, R., Nylin, S., Pitnick, S., Schoff, C., Signorelli, M., Teder, T. & Wiklund, C. (2007). Proximate causes of Rensch's rule: does sexual size dimorphism in arthropods result from sex differences in development time? Am. Nat. 169, 245-257.
Bonnet, X., Lorioux, S., Pearson, D., Aubret, F., Bradshaw, D., Delmas, V. & Fauvel, T. (2011). Which proximate factor determines sexual size dimorphism in tiger snakes? Biol. J. Linn. Soc. 103, 668-680.
Ceballos, C.P., Adams, D.C., Iverson, J.B. & Valenzuela, N. (2013). Phylogenetic patterns of sexual size dimorphism in turtles and their implications for Rensch's rule. Evol. Biol. 40, 194-208.
Cheverud, J.M., Dow, M.M. & Leutenegger, D. (1986). A phylogenetic autocorrelation analysis of sexual dimorphism in primates. Am. Anthropol. 88, 916-922.
Dale, J., Dunn, P.O., Figuerola, J., Lislevand, T., Székely, T. & Whittingham, L.A. (2007). Sexual selection explains Rensch's rule of allometry for sexual size dimorphism. Proc. Roy. Soc. Lond. Ser. B 274, 2971-2979.
Denoël, M., Ivanović, A., Džukić, G. & Kalezić, M.L. (2009). Sexual size dimorphism in the evolutionary context of facultative paedomorphosis: insights from European newts. BMC Evol. Biol. 9, 278.
Fairbairn, D.J. (1994). Sexual selection and the evolution of allometry for sexual size dimorphism in the water strider, Aquarius remigis. Am. Nat. 144, 101-118.
Fairbairn, D.J. (1997). Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annu. Rev. Ecol. Syst. 28, 659-687.
Ficetola, G.F., Scali, S., Denoël, M., Montinaro, G., Vukov, T.D., Zuffi, M.A.L. & Padoa-Schioppa, E. (2010). Ecogeographical variation of body size in the newt Triturus carnifex: comparing the hypotheses using an information-theoretic approach. Glob. Ecol. Biogeogr. 19, 485-495.
Ficetola, G.F., Bonardi, A., Colleoni, E., Padoa-Schioppa, E. & Scali, S. (2013). Evolution of sexual dimorphism in the number of tail vertebrae in salamanders: comparing multiple hypotheses. Evol. Biol. 40, 220-227.
Freckleton, R.P., Harvey, P.H. & Pagel, M. (2002). Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712-726.
Frýdlová, P. & Frynta, D. (2010). A test of Rensch's rule in varanid lizards. Biol. J. Linn. Soc. 100, 293-306.
Griffiths, R.A. (1995). Newts and salamanders of Europe. London: Poyser Natural History.
Gvoždík, L. & Damme, R.V. (2006). Triturus newts defy the running-swimming dilemma. Evolution 60, 2110-2121.
Herczeg, G., Gonda, A. & Merila, J. (2010). Rensch's rule inverted - female-driven gigantism in nine-spined stickleback Pungitius pungitius. J. Anim. Ecol. 79, 581-588.
Heyer, W.R., Donelly, M.A., McDiamid, R.W., Hayek, L.A.C. & Foster, M.S. (1994). Measuring and monitoring biological diversity. Standard methods for amphibians. Washington: Smithsonian Institution Press.
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. J. Zool. Syst. Evol. Res. 46, 381-387.
Lanza, B., Andreone, F., Bologna, M.A., Corti, C. & Razzetti, E. (2007). Fauna d'Italia. Vol. XLII, Amphibia: Bologna: Calderini.
Lanza, B., Arntzen, J.W. & Gentile, E. (2009). Vertebral numbers in the Caudata of the Western Palaeartic (Amphibia). Atti Mus. Civ. Stor. Nat. Trieste 54, 3-114.
Liao, W.B. & Chen, W. (2012). Inverse Rensch's rule in a frog with female-biased sexual size dimorphism. Naturwissenschaften 99, 427-431.
Liao, W.B., Zeng, Y., Zhou, C.Q. & Jehle, R. (2013). Sexual size dimorphism in anurans fails to obey Rensch's rule. Front. Zool. 10, 1-7.
Lovich, J.E. & Gibbons, J.W. (1992). A review of techniques for quantifying sexual size dimorphism. Growth Dev. Aging 56, 269-281.
Malmgren, J.C. (2001). Allometry for sexual size dimorphism in newts of the genus Triturus (Caudata: Salamandridae). PhD Thesis, Örebro University, Örebro.
Malmgren, J.C. & Thollesson, M. (1999). Sexual size and shape dimorphism in two species of newts, Triturus cristatus and T.vulgaris (Caudata: Salamandridae). J. Zool. (Lond.) 249, 127-136.
McIntire, E.J.B. & Fajardo, A. (2009). Beyond description: the active and effective way to infer processes from spatial patterns. Ecology 90, 46-56.
Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature 401, 877-884.
Paradis, E., Claude, J. & Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290.
Polak, J. & Frynta, D. (2009). Sexual size dimorphism in domestic goats, sheep, and their wild relatives. Biol. J. Linn. Soc. 98, 872-883.
Pyron, R.A. & Wiens, J.J. (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.
Rensch, B. (1960). Evolution above the species level. New York: Columbia University Press.
Revell, L.J. (2010). Phylogenetic signal and linear regression on species data. Methods Ecol. Evol. 1, 319-329.
Revell, L.J. (2012). Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223.
Serrano-Meneses, M.A., Cordoba-Aguilar, A., Azpilicueta-Amorin, M., Gonzalez-Soriano, E. & Székely, T. (2008). Sexual selection, sexual size dimorphism and Rensch's rule in Odonata. J. Evol. Biol. 21, 1259-1273.
Shine, R. (2000). Vertebral numbers in male and female snakes: the roles of natural, sexual and fecundity selection. J. Evol. Biol. 13, 455-565.
Sillero, N., Campos, J., Bonardi, A., Corti, C., Creemers, R., Crochet, P., Crnobrnja-Isailovic, J., Denoël, M., Ficetola, G.F., Gonçalves, J., Kuzmin, S., Lymberakis, P., 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. Amphib.-Reptil. 35, 1-31. doi: 10.1163/15685381-00002935.
Sokal, R.R. & Rohlf, F.J. (1995). Biometry. New York: W. H. Freeman and Company.
Székely, T., Freckleton, R.P. & Reynolds, J.D. (2004). Sexual selection explains Rensch's rule of size dimorphism in shorebirds. Proc. Natl Acad. Sci. USA 101, 12224-12227.
Verrel, P.A. (1985). Getting into a pickle with preserved specimens: formalin and distortion in the smooth newt, Triturus vulgaris. Herpetol. J. 1, 39-40.
Webb, T.J. & Freckleton, R.P. (2007). Only half right: species with female-biased sexual size dimorphism consistently break Rensch's rule. PLoS ONE 2, e897.
Wiens, J.J., Sparreboom, M. & Arntzen, J.W. (2011). Crest evolution in newts: implications for reconstruction methods, sexual selection, phenotypic plasticity and the origin of novelties. J. Evol. Biol. 24, 2073-2086.
Wiklund, C. & Forsberg, J. (1991). Sexual size dimorphism in relation to female polygamy and protandry in butterflies: a comparative study of Swedish Pieridae and Satyridae. Oikos 60, 373-381.
Zhang, L. & Lu, X. (2013). Sexual size dimorphism in anurans: ontogenetic determination revealed by an across-species comparison. Evol. Biol. 40, 84-91.