Sexual size dimorphism in ground squirrels (Rodentia: Sciuridae: Marmotini) does not correlate with body size and sociality
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
PubMed
23672689
PubMed Central
PMC3663772
DOI
10.1186/1742-9994-10-27
PII: 1742-9994-10-27
Knihovny.cz E-zdroje
- Publikační typ
- časopisecké články MeSH
INTRODUCTION: Sexual size dimorphism (SSD) is a widespread phenomenon in animals including mammals. It has been demonstrated that across species, the direction and magnitude of sexual dimorphism in body size often corresponds to social systems. Moreover, many animal lineages conform to "Rensch's rule", which states that male-biased SSD increases with body size. We tested whether considerable differences in sociality and large variation in body size were connected with the evolution of SSD in the structural body size of ground squirrels, an otherwise ecologically relatively homogenous group of terrestrial rodents. RESULTS: We found the general trend of male-biased SSD in ground squirrels, however, male size increases nearly perfectly isometrically with female size among species and sociality does not explain departures from this relationship. Species with different sociality grades significantly differ in body size, with the most social species tending to be the largest. CONCLUSIONS: We suggest that lack of conformity with Rensch´s rule in ground squirrels may be attributed to their low variation in SSD, and briefly discuss three potential causes of small magnitude of SSD in the structural size in rodents: low selection on SSD in structural dimensions, ontogenetic and genetic constraints and the existence of ecological/selection factors preventing the evolution of extensive SSD.
Zobrazit více v PubMed
Darwin CR. The descent of man and selection in relation to sex. London: John Murray; 1871.
Fairbairn DJ, Blanckenhorn WU, Szekely T. Sex, size, and gender roles: evolutionary studies of sexual size dimorphism. Oxford: Oxford University Press; 2007.
Lindenfors P, Gittelman JL, Jones KE. In: Sex, size, and gender roles: evolutionary studies of sexual size dimorphism. Fairbairn DJ, Blanckenhorn WU, Szekely T, editor. Oxford: Oxford University Press; 2007. Sexual size dimorphism in mammals; pp. 16–26.
Lindenfors P, Tullberg BS. Phylogenetic analyses of primate size evolution: the consequences of sexual selection. Biol J Linn Soc. 1998;64:413–447. doi: 10.1111/j.1095-8312.1998.tb00342.x. DOI
Lindenfors P, Tullberg BS, Biuw M. Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds. Behav Ecol Sociobiol. 2002;52:188–193. doi: 10.1007/s00265-002-0507-x. DOI
Pérez-Barbería FJ, Gordon IJ, Pagel M. The origins of sexual dimorphism in body size in ungulates. Evolution. 2002;56:1276–1285. PubMed
Rensch B. Die Abhängigkeit der relativen Sexualdifferenz von der Körpergrösse. Bonner Zool Beitr. 1950;1:58–69.
Fairbairn DJ. Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annu Rev Ecol Syst. 1997;28:659–687. doi: 10.1146/annurev.ecolsys.28.1.659. DOI
Abouheif E, Fairbairn DJ. A comparative analysis of allometry for sexual size dimorphism: assessing Rensch’s rule. Am Nat. 1997;149:340–362.
Starostová Z, Kubička L, Kratochvíl L. Macroevolutionary pattern of sexual size dimorphism in geckos corresponds to intraspecific temperature-induced variation. J Evol Biol. 2010;23:670–677. doi: 10.1111/j.1420-9101.2010.01933.x. PubMed DOI
Shulte-Hostedde AI. In: Rodent societies: An ecological and evolutionary perspective. Wolff JO, Sherman PW, editor. Chicago and London: The University of Chicago Press; 2007. Sexual size dimorphism in Rodents; pp. 115–128.
McKenna MC, Bell SK. Classification of mammals above the species level. New York: Columbia University Press; 1997.
Herron MD, Castoe TA, Parkinson CL. Sciurid phylogeny and the paraphyly of Holarctic ground squirrels (Spermophilus) Mol Phylogenet Evol. 2004;31:1015–1030. doi: 10.1016/j.ympev.2003.09.015. PubMed DOI
Fabre P-H, Hautier L, Dimitrov D, Douzery EJP. A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol Biol. 2012;12:88. doi: 10.1186/1471-2148-12-88. PubMed DOI PMC
Nowak RM. Walker’s mammals of the world. Baltimore and London: The Johns Hopkins University Press; 1999.
Bibikow DI. Die Murmeltiere der Welt. Heidelberg: Spektrum Akademischer Verlag; 1996.
Armitage KB. Sociality as a life-history tactic of ground squirrels. Oecol. 1981;48:36–49. doi: 10.1007/BF00346986. PubMed DOI
Michener GR. In: Advances in the Study of Mammalian Behavior. Eisenberg JF, Kleiman DG, editor. Lawrence: American Society of Mammalogists; 1983. Kin identification, matriarchies, and the evolution of sociality in ground-dwelling sciurids; pp. 528–572. [Special Publication No. 7]
Best TL, Titus AS, Caesar K, Lewis CL. Ammospermophilus harrisii. Mamm Species. 1990;366:1–7.
Best TL, Caesar K, Titus AS, Lewis CL. Ammospermophilus insularis. Mamm Species. 1990;364:1–4.
Best TL, Lewis CL, Caesar K, Titus AS. Ammospermophilus interpres. Mamm Species. 1990;365:1–6.
Belk MC, Smith DH. Ammospermophilus leucurus. Mamm Species. 1991;368:1–8.
Helgen KM, Cole RF, Helgen LE, Wilson DE. Generic revision in the holoarctic ground squirrels genus Spermophilus. J Mamm. 2009;90:270–305. doi: 10.1644/07-MAMM-A-309.1. DOI
Ceballos G, Wilson DE. Cynomys mexicanus. Mamm Species. 1985;248:1–3.
Linzey AV, Rosmarino N, Willson K, Roth E, Hammerson G, Cannings S. IUCN Red List of Threatened Species. Version 2010.4. IUCN; 2010. Cynomys parvidens. [ http://www.iucnredlist.org]
Blumstein DT, Armitage KB. Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls. Am Nat. 1997;150:179–200. doi: 10.1086/286062. PubMed DOI
Allainé D. Sociality, mating system and reproductive skew in marmots: evidence and hypotheses. Behav Process. 2000;51:21–34. doi: 10.1016/S0376-6357(00)00116-9. PubMed DOI
Oaks E, Young PJ, Kirkland GL, Schmidt DF. Spermophilus variegatus. Mamm Species. 1987;272:1–8.
Popov VS. Rol’ social’nyh svjazej v prostranstvennoj strukture poselenija zheltogo suslika. [The role of social relationships in the spatial structure of the colony in the yellow ground squirrel (Spermophilus fulvus Licht. 1823)] PhD thesis. Moscow State University; 2007.
Kucheruk VV, Khlyap LA. Lagomorphs and Rodents of Middle Asia (Zairseobraznye I Gryzuny Sredney Azii) Moscow: Geos; 2005.
Soldatova AN. Vlijanie plotnosti naselenia na charakter ispolzovanija territorii malym suslikom [Effect of population density on the character of the utilization of home ranges by Citellus pygmaeus Pall.] Zool Zh. 1962;41:913–921.
Kryštufek B, Vohralík V. Mammals of Turkey and Cyprus, Vol. 2, Rodentia I: Sciuridae, Dipodidae, Gliridae, Arvicolinae. Koper: Science and Research Centre of the Republic of Slovenia; 2005.
Gür MK, Gür H. Spermophilus xanthoprymnus. Mamm Species. 1995;864:183–194.
Best TL. Spermophilus mohavensis. Mamm Species. 1995;509:1–7.
Webb TJ, Freckleton RP. Only half right: species with female-biased sexual size dimorphism consistently break Rensch's rule. PLoS One. 2007;2:e897. doi: 10.1371/journal.pone.0000897. PubMed DOI PMC
Tubaro PL, Bertelli S. Female-biased sexual size dimorphism in tinamous: a comparative test fails to support Rensch's rule. Biol J Linn Soc. 2003;80:519–527. doi: 10.1046/j.1095-8312.2003.00252.x. DOI
Stuart-Fox D. A test of Rensch’s rule in dwarf chameleons (Bradypodion spp.), a group with female-biased sexual size dimorphism. Evol Ecol. 2009;23:425–433. doi: 10.1007/s10682-008-9242-8. DOI
Reiss MJ. Sexual dimorphism in body size: Are larger species more dimorphic? J Theor Biol. 1986;121:163–172. doi: 10.1016/S0022-5193(86)80090-X. DOI
Székely T, Lislevand T, Figuerola J. In: Sex, size and gender roles. Fairbairn D, Székely T, Blackenhorn W, editor. Oxford: Oxford University Press; 2007. Sexual size dimorphism in birds; pp. 27–37.
Lacey EA, Wieczorek JR. Territoriality and male reproductive success in arctic ground squirrels. Behav Ecol. 2001;12:626–632. doi: 10.1093/beheco/12.5.626. DOI
Hoogland JL. Sexual dimorphism of prairie dogs. J Mamm. 2003;84:1254–1266. doi: 10.1644/BME-008. DOI
Schwagmeyer PL. Scramble-competition polygyny in an asocial mammal: Male mobility and mating success. Am Nat. 1988;131:885–892. doi: 10.1086/284828. DOI
Polák J, Frynta D. Sexual size dimorphism in domestic goats, sheep, and their wild relatives. Biol J Linn Soc. 2009;98:872–883. doi: 10.1111/j.1095-8312.2009.01294.x. DOI
Frynta D, Baudyšová J, Hradcová P, Faltusová K, Kratochvíl L. Allometry of sexual size dimorphism in domestic dog. PLoS One. 2012;7:e46125. doi: 10.1371/journal.pone.0046125. PubMed DOI PMC
Maynard-Smith J. The evolution of sex. Cambridge: Cambridge University Press; 1978.
Lande R. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution. 1980;34:292–305. doi: 10.2307/2407393. PubMed DOI
Dobson FS, Michener GR. Maternal traits and reproduction in Richardson's ground squirrels. Ecology. 1995;76:851–862. doi: 10.2307/1939350. DOI
Huber S, Millesi E, Walzl M, Dittami J, Arnold W. Reproductive effort and costs of reproduction in female European ground squirrels. Oecologia. 1999;121:19–24. doi: 10.1007/s004420050902. PubMed DOI
Sauer JR, Slade NA. Uinta ground squirrel demography: is body mass a better categorical variable than age? Ecology. 1987;68:642–650. doi: 10.2307/1938469. DOI
Barash D. Marmots: Social behavior and ecology. Stanford: Stanford University Press; 1989.
Hoogland JL. Cynomys ludovicianus. Mamm Species. 1996;535:1–10.
Hayssen V. Patterns of body and tail length and body mass in Sciuridae. J Mamm. 2008;89:852–873. doi: 10.1644/07-MAMM-A-217.1. DOI
Thorington RW, Jr, Koprowski JL, Steele MA, Whatton JF. Squirrels of the World. Baltimore: The John Hopkins University Press; 2012.
Gür H. Why do Anatolian ground squirrels exhibit a Bergmannian size pattern? A phylogenetic comparative analysis of geographic variation in body size. Biol J Linn Soc. 2010;100:695–710. doi: 10.1111/j.1095-8312.2010.01447.x. DOI
Millesi E, Strijkstra AM, Hoffmann IE, Ditami JP, Daan S. Sex and age differences in mass, morphology, and annual cycle in European ground squirrels, Spermophilus citellus. J Mamm. 1999;80:218–231. doi: 10.2307/1383222. DOI
Zimmerman EG. Growth and age determination in the thirteen-lined ground squirrel, Spermophilus tridecemlineatus. Am Midl Nat. 1972;87:314–325. doi: 10.2307/2423564. DOI
Turner BN, Iverson SL, Severson KL. Postnatal growth and development of captive franklin's ground squirrels (Spermophilus franklinii) Am midl nat. 1976;95:93–102. doi: 10.2307/2424236. DOI
Kratochvíl L, Fokt M, Rehák I, Frynta D. Misinterpretation of character scaling: A tale of sexual dimorphism in body shape of common lizards. Can J Zool. 2003;81:1112–1117. doi: 10.1139/z03-078. DOI
Waterman JM. In: Rodent Societes: an ecological and evolutionary perspective. Wolff JO, Sherman PW, editor. Chicago and London: The University of Chicago Press; 2007. Male mating strategies in rodents; pp. 27–41.
Rowell TE. Beyond the one-male group. Behaviour. 1988;104:189–201. doi: 10.1163/156853988X00511. DOI
Martins EP, Hansen TF. Phylogenies and the comparative method: A general approach to incorporating phylogenetic information into analysis of interspecific data. Am Nat. 1997;149:646–667. doi: 10.1086/286013. DOI
Felsenstein J. Phylogenies and the comparative method. Am Nat. 1985;125:1–15. doi: 10.1086/284325. DOI
Pagel MD. In: Morphology, shape and phylogeny. MacLeod N, Foley PL, editor. London: Taylor & Francis; 2002. Modelling the evolution of continuously varying characters on phylogenetic trees; pp. 269–286.
Best TL, Titus AS, Lewis CL, Caesar K. Ammospermophilus nelsoni. Mamm Species. 1990;367:1–7.
Díaz-Uriarte R, Garland T. Effects of branch length errors on the performance of phylogenetically independent contrasts. Syst Biol. 1998;47:654–672. doi: 10.1080/106351598260653. PubMed DOI
Díaz-Uriarte R, Garland T. Testing hypotheses of correlated evolution using phylogenetically independent contrasts: Sensitivity to deviations from Brownian motion. Syst Biol. 1996;45:27–47. doi: 10.1093/sysbio/45.1.27. DOI
Revell LJ. Phylogenetic signal and linear regression on species data. Meth Ecol Evol. 2010;1:319–329. doi: 10.1111/j.2041-210X.2010.00044.x. DOI
Capellini I, Venditti C, Barton RA. Phylogeny and metabolic scaling in mammals. Ecology. 2010;91:2783–2793. doi: 10.1890/09-0817.1. PubMed DOI
Capellini I, Venditti C, Barton RA. Placentation and maternal investment in mammals. Am Nat. 2011;177:86–98. doi: 10.1086/657435. PubMed DOI
Matthews LJ, Amold C, Machanda Z, Nunn CL. Primate extinction risk and historical patterns of speciation and extinction in relation to body mass. Proc R Soc B. 2011;278:1256–1263. doi: 10.1098/rspb.2010.1489. PubMed DOI PMC
Midford PET, Garland T, Maddison WP. PDAP Package of Mesquite. Version 1.07. [ http://mesquiteproject.org]
Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis. Version 2.75. [ http://mesquiteproject.org]
Martins EP. COMPARE, Computer programs for the statistical analysis of comparative data. version 4.6b. [ http://compare.bio.indiana.edu/]
Pagel M, Meade A. BayesTraits version 1.0 computer package. [ http://www.evolution.rdg.ac.uk]
Absolute, not relative brain size correlates with sociality in ground squirrels