Abstract
Sexual size dimorphism (SSD) is affected by a large number of factors, mating system being one of the most relevant. Almost 70 species of subterranean rodents of the genus Ctenomys are considered highly polygynic, and polygyny jointly with absence of paternal care of the young, favours high SSD. In this respect, Rensch’s rule predicts that SSD scales with body size so that when males are larger than females SSD tends to increase with body size. We studied SSD and Rensch’s rule in 28 taxa of Ctenomys using a phylogenetic approach employing the method of phylogenetic reduced major axis (pRMA) to perform reduced major axis (RMA) model II regression in the form of log 10(male mass) on log 10(female mass). The RMA regression slope (β) was statistically tested to accept or reject the null hypothesis that βpRMA= 1.0. A slope significantly >1.0 would signal concordance with Rensch’s rule. Our results showed that despite a high degree of male-biased SSD as expected from polygynic species, Rensch’s rule is not verified in this rodent group. The causes of the non-concordance with Rensch’s rule as well as its taxonomic level of application are discussed in terms of current models of SSD.
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Abouheif, E., Fairbairn, D.J., 1997. A comparative analysis ofallometry for sexual size dimorphism: assessing Rensch’s rule. Am. Nat. 149, 540–562.
Anderson, S., 1997. Mammals of Bolivia: taxonomy and distribution. Bull. Am. Mus. Nat. Hist. 234, 1–652.
Andersson, M., 1994. Sexual Selection. Princeton University Press, Princeton.
Beery, A.K., Lacey, E.A., Francis, D.D., 2008. Oxytocin and vasopressin receptors distributions in a solitary and a social species of tuco-tuco (Ctenomys haigi and Ctenomys sociabilis).J. Comp. Neurol. 507, 1847–1859.
Begall, S., Burda, H., Schleich, C.E. (Eds.), 2007. Subterranean Rodents: News from Underground. Springer-Verlag, Berlin-Heidelberg.
Bidau, C.J., Martí, D.A., 2008a. Rensch’s rule in Dichroplus pratensis: a reply to Wolak. Ann. Entomol. Soc. Am. 101, 802–803.
Bidau, C.J., Martí, DA, 2008b. Contrasting patterns of sexual size dimorphism in the grasshoppers Dichroplus vittatus and D pratensis (Acrididae, Melanoplinae). J. Orthop. Res. 17, 201–211.
Bidau, C.J., Martí, D.A., Castillo, E.R., 2013. Rensch’s rule is not verified in melanopline grasshoppers (Acrididae). J. Insect. Biodivers. 1 (12), 1–14.
Bidau, C.J., Medina, A.I., 2013. Sexual size dimorphism and testis size allometry in tuco-tucos (Rodentia: Ctenomyidae). Mammalia 77, 81–93.
Bidau, C.J., 2006. Familia Ctenomyidae. In: Bárquez, R., Díaz, M.M., Ojeda, R. (Ed.), Mamíferos de Argentina. Sistemática y Distribución Sociedad Argentina para el Estudio de los Mamiferos. Tucumán, Argentina, pp. 212–231.
Bidau, C.J., 2014. Genus Ctenomys. In: Patton, J.L., Pardiñas, U.F.J., D’Elía, G. (Eds.), Mammals of South America. Rodents, vol. 2. The University of Chicago Press, Chicago, IL
Blanckenhorn, W.U., Meier, R., Teder, T., 2007. Rensch’s rule in insects: patterns among and within species. In: Fairbairn, D.J., Blanckenhorn, W.U., Székely, T. (Ed.), Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press, Oxford, pp. 60–70.
Blanckenhorn, W.U., Stillwell, R.C., Young, K.A., Fox, C.W., Ashton, K.G., 2006. When Rensch meets Bergmann: does sexual size dimorphism change systematically with latitude? Evolution 60, 2004–2011.
Blomberg, S.P., Garland, T., Ives, A.R., 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745.
Bondrup-Nielsen, S., Ims, R.A., 1990. Reversed sexual size dimorphism in microtines: are females larger than males or are males smaller than females? Evol. Ecol. 4, 261–272.
Carranza, J., 2009. Defining sexual selection as sex-dependent selection. Anim. Behav. 77, 749–751.
Carranza, J., 2010. Sexual selection and the evolution of evolutionary theories. Anim. Behav. 79, e5–e6.
Clarke, M.R.B., 1980. The reduced major axis of a bivariate sample. Biometrika 67, 441–446.
Clutton-Brock, T., 2007. Sexual selection in males and females. Science 318, 1882–1885.
Clutton-Brock, T., 2009. Sexual selection in females. Anim. Behav. 77, 2–11.
Clutton-Brock,T., 2010. We do not need asexual selection 2.0- nor a theory of genial selection. Anim. Behav. 79, e7–e10.
Dale, J., Dunn, P.O., Figuerola, J., Lislevand, T., Székely, T., Wittingham, L.A., 2007.
Sexual selection explains Rensch’s rule of allometry for sexual size dimorphism. Proc. R. Soc. Lond. B 4, 2971–2979.
Darwin, C, 1859. On the Origin of Species by Means of Natural Selection. John Murray, London.
Darwin, C, 1871. The Descent of Man and Selection in Relation to Sex. John Murray, London.
Fairbairn, D.J., 1997. Allometry for sexual size dimorphism, patterns and processes in the coevolution of body size in males and females. Ann. Rev. Ecol. Syst. 28, 659–687.
Fairbairn, D.J., 2007. Introduction: the enigma of sexual size dimorphism. In: Fairbairn, D.J., Blanckenhorn, W.U., Székely, T. (Ed.), Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press, Oxford, pp. 1–10.
Fairbairn, D.J., 2013. Odd Couples: Extraordinary Differences between the Sexes in the Animal Kingdom. Princeton University Press, Princeton.
Fairbairn, D.J., Blanckenhorn, W.U., Székely, T. (Eds.), 2007. Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press, Oxford.
Felsenstein, J., 1985. Phylogenies and the comparative method. Am. Nat. 125, 1–15.
Fisher, R.A., 1930. The Genetical Theory of Natural Selection. Oxford University Press, Oxford.
Frynta, D., Baudysová, J., Hradcová, P., Faltusová, K., Kratochvíl, L., 2012. Allometry of sexual size dimorphism in domestic dog. PLoS ONE 7 (9), e46125.
Giménez, M.D., Mirol, P., Bidau, C.J., Searle, J.B., 2002. Molecular analysis of populations of Ctenomys (Caviomorpha, Rodentia) with high karyotypic variability. Cytogenet. Genome Res. 96, 130–136.
Gordon, A.D., 2006. Scaling of size and dimorphism in Primates II. Macroevolution. Int. J. Primatol. 27, 63–105.
Gardner, S.L., Salazar-Bravo, J., Cook, J.A., 2014. New species of Ctenomys Blainville 1826 (Rodentia: Ctenomyidae) from the lowlands and central valleys of Bolivia. In: Special Publications. Museum of Texas Tech University, Number 62, pp. 1–34.
Graziani, R.N., Lacey, E.A., 2004. A molecular analysis of the mating system of the Patagonian tuco-tuco (Ctenomys haigi). In: Abstracts 84th Annual Meeting of the American Society of Mammalogists, Arcata, CA, Poster 223.
Hayssen, V., 2008. Patterns of body and tail length and body mass in Sciuridae. J. Mammal. 89, 852–873.
Isaac, J.L., 2005. Potential causes and life-history consequences of sexual size dimorphism in mammals. Mammal. Rev. 35, 101–115.
Kelt, D.A., Gallardo, M.H., 1994. A new species of tuco-tuco, genus Ctenomys (Rodentia, Ctenomyidae) from Patagonian Chile. J. Mammal. 75, 338–348.
Kokko, K., Jennions, M.D., Brooks, R., 2006. Unifying and testing models of sexual selection. Annu. Rev. Ecol. Evol. Syst. 37, 43–66.
Kupfer, A., 2007. Sexual size dimorphism in amphibians: and overview. In: Fairbairn, D.J., Blanckenhorn, W.U., Székely, T. (Ed.), Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press, Oxford, pp. 50–59.
Lacey, E.A., Patton, J., Cameron, G.N. (Eds.), 2000. Life Underground: The Biology of Subterranean Rodents. The University of Chicago Press, Chicago.
Leutenegger, W., Cheverud, J., 1982. Correlates of sexual dimorphism in Primates: ecological and size variables. Int. J. Primatol. 3, 387–402.
Lindenfors, P., Gittleman, J.L., Jones, K.E., 2007. Sexual size dimorphism in mammals. In: Fairbairn, D.J., Blanckenhorn, W.U., Székely, T. (Ed.), Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press, Oxford, pp. 16–26.
Lovich, J.E., Gibbons, J.W., 1992. A review of techniques for quantifying sexual size dimorphism. Growth Dev. Aging 56, 269–281.
Lu, D., Zhou, C.Q., Liao, W.B., 2014. Sexual size dimorphism lacking in small mammals. Northwest. J. Zool. 10, 53–59.
Luna, F., Antinuchi, CD., Busch, C, 2002. Digging energetics in the South American rodent Ctenomystalarum (Rodentia, Ctenomyidae). Can. J. Zool. 80, 2144–2149.
Martinez, P.A., Ferreira Amado, T.F., Bidau, C.J., 2014. A phylogenetic approach to the study of sexual size dimorphism in Felidae and an assessment of Rensch’s rule. Ecosistemas 23, 27–36.
Mateju, J., Kratochvil, L, 2013. Sexual size dimorphism in ground squirrels (Rodentia: Sciuridae: Marmotini) does not correlate with body size and sociality. Front. Zool. 10, 27.
Maynard-Smith,J., 1982. Evolution and the Theory of Games. Cambridge University Press, Cambridge.
Maynard-Smith, J., 1998. Evolutionary Genetics, 2nd Edn. Oxford University Press, Oxford.
McCardle, B.H., 1988. The structural relationship: regression in biology. Can. J. Zool. 66, 2329–2339.
McNab, B.C., 1979. The influence of body size on the energetics and distribution of fossorial and burrowing mammals. Ecology 5, 1010–1021.
Medina, A.I., Martí, D.A., Bidau, C.J., 2007. Subterranean rodents of the genus Ctenomys (Caviomorpha, Ctenomyidae) follow the converse to Bergmann’s rule. J. Biogeogr. 34, 1439–1454.
Mirol, P., Giménez, M.D., Searle, J.B., Bidau, C.J., Faulkes, C.G., 2010. Population and species boundaries in the South American subterranean rodent Ctenomys in a dynamic environment. Biol. J. Linn. Soc. 100, 368–383.
Moors, P.J., 1980. Sexual dimorphism in the body size of mustelids (Carnivora): the role of food habits and breeding systems. Oikos34, 147–158.
Nandini, R., (PhD Dissertation) 2011. Evolution of Sexual Size Dimorphism in Squirrels. Auburn University, Alabama, USA.
Nevo, E., 1979. Adaptive convergence and divergence of subterranean mammals. Annu. Rev. Ecol. Syst. 10, 269–308.
Nevo, E., 1999. Mosaic Evolution of Subterranean Mammals: Regression, Progression and Global Convergence. Oxford University Press, Oxford.
Nevo, E., Beiles, A., Heth, G., Simson, S., 1986. Adaptive differentiation of body size in speciating mole rats. Oecologia 69, 327–333.
Osgood, W.H., 1943. The mammals of Chile. Field Mus. Nat. Hist. Zool. Ser. 29, 191–204.
Parada, A., D’elía, G., Bidau, C.J., Lessa, E., 2011. Species groups and the evolutionary diversification of tuco-tucos, genus Ctenomys (Rodentia, Ctenomyidae). J. Mammal. 92, 671–682.
Pearson, O.P., 1984. Taxonomy and natural history of some fossorial rodents of Patagonia, southern Argentina. J. Zool. 202, 225–237.
Pearson, O.P., Christie, M.I., 1985. Los tuco-tucos (género Ctenomys) de los Parques Nacionales Lanín y Nahuel Huapi, Argentina. Hist. Nat. 5, 337–343.
Pine, R.H., Angle, J.P., Schamberger, M.L., 1979. Contributions to the mammalogy of Chile. Mammalia 43, 649–655.
Polák, J., Frynta, D., 2010. Patterns of sexual size dimorphism in cattle breeds support Rensch’s rule. Evol. Ecol. 24, 1255–1266.
Ralls, K., 1976. Mammals in which females are larger than males. Q. Rev. Biol. 51, 245–276.
Ralls, K., Mesnick, S.L., 2009. Sexual dimorphism. In: Perrin, W.F., Würsig, B., Thewissen, J.G.M.(Eds.), Encyclopedia of Marine Mammals. Academic Press, Burlington, pp. 1011–1105.
Reig, O.A., Busch, C, Ortells, M.O., Contreras, J.R., 1990. An overview of evolution, systematics, population, biology, cytogenetics molecular biology and speciation in Ctenomys. In: Nevo, E., Reig, O.A. (Ed.), Evolution of Subterranean Mammals at the Organismal and Molecular Levels. Alan R. Liss, New York, pp. 71–96.
Reiss, M.J., 1986. Sexual dimorphism in body size: are larger species more dimorphic? J. Theor. Biol. 121, 163–172.
Reiss, M.J., 1989. The Allometry of Growth and Reproduction. Cambridge University Press, London.
Remes, V., Székely, T., 2010. Domestic chickens defy Rensch’s rule: sexual size dimorphism in chicken breeds. J. Evol. Biol. 23, 2754–2759.
Rensch, B., 1950. Die Abhängigkeit der relativenSexualdifferenz von der Körpegrosse. Bonner ZoologischeBeitraege 1, 58–69.
Rensch, B., 1960. Evolution Above the Species Level. Columbia University Press, New York.
Revell, L.J., 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223.
Rocha-Barbosa, O., Bernardo, J.S.L., Loguercio, M.F.C., Freitas, T.R.O., Santos-Mallet, J.R., Bidau, C.J., 2013. Penial morphology in three species of Brazilian tuco-tucos, Ctenomys torquatus, C minutes, and Cflamarioni (Rodentia: Ctenomyidae). Braz. J. Biol. 73, 201–209.
Roughgarden, J., Akcay, E., 2010. Do we need a sexual selection 2.0? Anim. Behav. 79, e1–e4.
Rosvall, K.A., 2011. Intrasexual competition in females: evidence for sexual selection? Behav. Ecol. 22, 1131–1140.
Russell, R.J., Baker, R.H., 1955. Geographic Variation in the Pocket Gopher, Cratogeomys castanops. Univ. Kansas Pub., Coahuila, México, pp. 591–608.
Schulte-Hostedde, A.I., 2007. Sexual size dimorphism in rodents. In: Wolff, J.O., Sherman, P.W. (Ed.), Rodent Societies: An Ecological and Evolutionary Perspective. The Chicago University Press, Chicago, pp. 115–118.
Shine, R., 1991. Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. Am. Nat. 138, 103–122.
Shuker, D.M., 2010. Sexual selection: endless forms or tangled bank? Anim. Behav. 79, e11–e17.
Smith, R.J., 1999. Statistics of sexual size dimorphism. J. Hum. Evol. 36, 423–459.
Smith, R.J., 2009. Use and misuse of the reduced major axis for line-fitting. Am. J. Phys. Anthropol. 140, 476–486.
Smorkatcheva, A.V., Lukhtanov, V.A., 2014. Evolutionary association between subterranean lifestyle and female sociality in rodents. Mammal. Biol. 79, 101–109.
Székely, T., Lislevand, T., Figuerola, J., 2007. Sexual size dimorphism in birds. In: Fairbairn, D.J., Blanckenhorn, W.U., Székely, T. (Ed.), Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press, Oxford, pp. 27–37.
Tassino, B., Estevana, I., Garberoa, R.P., Altesora, P., Lacey, E.A., 2011. Space use by Rio Negro tuco-tucos (Ctenomys rionegrensis): excursions and spatial overlap. Mammal. Biol. 76, 143–147.
Tubaro, P.L., Bertelli, S., 2003. Female-biased sexual size dimorphism in tinamous, a comparative test fails to support Rensch’s rule. Biol. J. Linn. Soc. 80, 519–527.
Vleck, D., 1979. The energy cost of burrowing by the pocket gopher Thomomys bottae. Physiol. Zool. 52, 122–138.
Wallace, A.R., 1889. Darwinism: An Exposition of the Theory of Natural Selection, With Some of Its Applications. Macmillan, London.
Webb, T.J., Freckleton, R.P., 2007. Only half right: species with female-biased sexual size dimorphism consistently break Rensch’s rule. PLoS ONE 8, e897.
Weckerly, P.W., 1998. Sexual size dimorphism: influence of mass and mating system in the most dimorphic mammals. J. Mammal. 79, 35–52.
Wu, H., Jiang, T., Huang, X., Lin, H., Wang, H., Wang, L., Niu, H., Feng, J., 2014. A test of Rensch’s rule in Greater Horseshoe Bat (Rhinolophus ferrumequinum) with female-biased sexual size dimorphism. PLoS ONE 9 (1), e86085.
Zenuto, R.R., 2010. Dear enemy relationships in the subterranean rodent Ctenomys talarum: the role of familiar odours. Anim. Behav. 79, 1247–1255.
Zenuto, R.R., Estavillo, C, Fanjul, M.S., 2007. Familiarity and mating behavior in the subterranean rodent Ctenomys talarum (tuco-tuco). Can. J. Zool. 85, 944–955.
Zenuto, R.R., Lacey, E.A., Busch, C, 1999a. DNA fingerprinting reveals polygyny in the subterranean rodent Ctenomys talarum. Mol. Ecol. 8, 1529–1532.
Zenuto, R.R., Malizia, E.E., Busch, C, 1999b. Sexual size dimorphism, testes size and mating system in two populations of Ctenomys talarum (Rodentia: Octodonti-dae). J. Nat. Hist. 33, 305–314.
Zhang, T., Nevo, E., Tang, l., Su, J., Lin, G., 2012. Plateau zokors on the Qinghai-Tibetan Plateau follow Bergmann’s rule latitudinally, but not altitudinally. Mamm. Biol. 77, 108–112.
Zelová, J., Šumbera, R., Okrouhlík,J., Burda, H., 2010. Cost of digging is determined by intrinsic factors rather than by substrate quality in two subterranean rodent species. Physiol. Behav. 99, 54–58.
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Martínez, P.A., Bidau, C.J. A re-assessment of Rensch’s rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach. Mamm Biol 81, 66–72 (2016). https://doi.org/10.1016/j.mambio.2014.11.008
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DOI: https://doi.org/10.1016/j.mambio.2014.11.008