BACKGROUND: The tendency for male-larger sexual size dimorphism (SSD) to scale with body size - a pattern termed Rensch's rule - has been empirically supported in many animal lineages. Nevertheless, its theoretical elucidation is a subject of debate. Here, we exploited the extreme morphological variability of domestic dog (Canis familiaris) to gain insights into evolutionary causes of this rule. METHODOLOGY/PRINCIPAL FINDINGS: We studied SSD and its allometry among 74 breeds ranging in height from less than 19 cm in Chihuahua to about 84 cm in Irish wolfhound. In total, the dataset included 6,221 individuals. We demonstrate that most dog breeds are male-larger, and SSD in large breeds is comparable to SSD of their wolf ancestor. Among breeds, SSD becomes smaller with decreasing body size. The smallest breeds are nearly monomorphic. CONCLUSIONS/SIGNIFICANCE: SSD among dog breeds follows the pattern consistent with Rensch's rule. The variability of body size and corresponding changes in SSD among breeds of a domestic animal shaped by artificial selection can help to better understand processes leading to emergence of Rensch's rule.

Department of Zoology Faculty of Science Charles University Prague Prague Czech Republic

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Darwin CR (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: John Murray. 432 p. PubMed PMC

Darwin CR (1868) The variation of animals and plants under domestication. London: John Murray. 2 vols..

Herre W (1980) Grundfragen zoologischer Domestikations-forschung. Nova Acta Leopold 241: 1–16.

Trut LN (1999) Early canid domestication: The farm-fox experiment. Am Sci 87: 160–169.

Sol D (2008) Artificial selection, naturalization, and fitness: Darwin’s pigeons revisited. Biol J Linn Soc 93: 657–665.

Drake AG, Klingenberg CP (2010) Large-scale diversification of skull shape in domestic dogs: disparity and modularity. Am Nat 175: 289–301. PubMed

Savolainen P, Leitner T, Wilton AN, Matisoo-Smith E, Lundeberg J (2004) A detailed picture of the origin of the Australian dingo, obtained from the study of mitochondrial DNA. Proc Natl Acad Sci USA 101: 12387–12390. PubMed PMC

Moehlman PD, Hofer H (1997) Cooperative breeding, reproductive suppression, and body mass in canids. In: Solomon NG, French JA, editors. Cooperative breeding in mammals. Cambridge: Cambridge University Press. 76–127.

Schmidt-Nielsen K (1984) Scaling: Why is animal size so important? Cambridge: Cambridge University Press. 241 p.

Isaac JL (2005) Potential causes and life-history consequences of sexual size dimorphism in mammals. Mamm Rev 35: 101–115.

Wayne RK (1986) Cranial morphology of domestic and wild canids: the influence of development on morphological change. Evolution 40: 243–261. PubMed

Chase K, Carrier DR, Adler FR, Ostrander EA, Lark KG (2005) Interaction between the X chromosome and an autosome regulates size sexual dimorphism in Portuguese water dogs. Gen Res 15: 1820–1824. PubMed PMC

Wang W, Ewen F, Kirkness EF (2005) Short interspersed elements (SINEs) are a major source of canine genomic diversity. Gen Res 15: 1798–1808. PubMed PMC

Sutter NB, Bustamante CD, Chase K, Gray MM, Zhao K, et al. (2007) A single IGF1 allele is a major determinant of small size in dogs. Science 316: 112–115. PubMed PMC

Gray MM, Sutter NB, Ostrander EA, Wayne RK (2010) The IGF1 small dog haplotype is derived from Middle Eastern grey wolves. BMC Biol 8: 16. PubMed PMC

Boyko AR, Quignon P, Li L, Schoenebeck JJ, Degenhardt JD, et al. (2010) A simple genetic architecture underlies morphological variation in dogs. PLOS Biology 8: e1000451. PubMed PMC

Shearin AL, Ostrander EA (2010) Canine morphology: hunting for genes and tracking mutations. PLoS Biol 8: e1000310. PubMed PMC

Darwin CR (1871) The descent of man, and selection in relation to sex. London: John Murray. 399 p.

Andersson M (1994) Sexual selection. Princeton University Press. 336 p.

Abouheif E, Fairbairn DJ (1997) A comparative analysis of allometry for sexual size dimorphism: assessing Rensch’s rule. Am Nat 149: 540–562.

Rensch B (1950) Die Abhangigkeit der relativen Sexualdifferenz von der Körpergröße. Bonn Zool Beitr 1: 58–69.

Rensch B (1959) Evolution above the species level. London: Methuen and Co. Ltd. 419 p.

Colwell RK (2000) Rensch’s rule crosses the line: convergent allometry of sexual size dimorphism in hummingbirds and flower mites. Am Nat 156: 495–510. PubMed

Kratochvíl L, Frynta D (2002) Body size, male combat and the evolution of sexual dimorphism in eublepharid lizards (Squamata: Eublepharidae). Biol J Linn Soc 76: 303–314.

Kratochvíl L, Frynta D (2007) Phylogenetic analysis of sexual dimorphism in eye-lid geckos (Eublepharidae): the effects of male combat, courtship behaviour, egg size, and body size. In: Fairbairn D, Székely T, Blanckenhorn W, editors.Sex, size and gender roles. Oxford University Press. 154–162.

Cox RM, Butler MA, John-Alder HB (2007) Sexual size dimorphism in reptiles. In: Fairbairn D, Székely T, Blanckenhorn W, editors. Sex, size and gender roles. Oxford University Press. 38–49.

Dale J, Dunn PO, Figuerola J, Lislevand T, Székely T, et al. (2007) Sexual selection explains Rensch’s rule of allometry for sexual size dimorphism. Proc R Soc B 274: 2971–2979. PubMed PMC

Székely T, Lislevand T, Figuerola J (2007) Sexual size dimorphism in birds. In: Fairbairn D, Székely T, Blanckenhorn W, editors. Sex, size and gender roles. Oxford University Press. 27–37.

Lindenfors P, Gittleman JL, Jones KE (2007) Sexual dimorphism in mammals. In: Fairbairn D, Székely T, Blanckenhorn W, editors. Sex, size and gender roles. Oxford University Press. 16–26.

Fairbairn DJ (1997) Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Ann Rev Ecol Syst 28: 659–687.

Webb TJ, Freckleton RP (2007) Only half right: species with female-biased dimorphism consistently break Rensch’s rule. PlosOne 2007: 1–10. PubMed PMC

Stephens PR, Wiens JJ (2009) Evolution of sexual size dimorphisms in emydid turtles: ecological dimorphism, Rensch’s rule, and sympatric divergence. Evolution 63: 910–25. PubMed

Fairbairn DJ, Preziosi RF (1994) Sexual selection and the evolution of allometry for sexual size dimorphism. Am Nat 144: 101–118.

Blanckenhorn WU, Stillwell RC, Young KA, Fox CW, Ashton KG (2006) When Rensch meets Bergmann: Does sexual size dimorphism change systematically with latitude? Evolution 60: 2004–2011. PubMed

Starostová Z, Kubička L, Kratochvíl L (2010) Macroevolutionary pattern of sexual size dimorphism in geckos corresponds to intraspecific temperature-induced variation. J Evol Biol 23: 670–677. PubMed

Walker SPW, McCormick MI (2009) Sexual selection explains sex-specific growth plasticity and positive allometry for sexual size dimorphism in a reef fish. Proc R Soc B 276: , 3335–3343. PubMed PMC

Remeš V, Székely T (2010) Domestic chickens defy Rensch’s rule: sexual size dimorphism in chicken breeds. J Evol Biol 23: 2754–2759. PubMed

Féderation Cynologique Internationale (2008) Nomenclature et Standards. Available: http://www.fci.be. Accessed 2008, Aug 15.

Sutter NB, Mosher DM, Gray MM, Ostrander EA (2008) Morphometrics within dog breeds are highly reproducible and dispute Rensch’s rule. Mamm Gen 19: 713–723. PubMed PMC

Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, et al. (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438: 803–819. PubMed

Vilá C, Maldonado JE, Wayne RK (1999) Phylogenetic relationships, evolution, and genetic diversity of the domestic dog. J Hered 90: 71–77. PubMed

Vilá C, Savolainen P, Maldonado JE, Amorim IR, Rice JE, et al. (1997) Multiple and ancient origins of the domestic dog. Science 276: 1687–1689. PubMed

Leonard JA, Wayne RK, Wheeler J, Valadez R, Guillén S, et al. (2002) Ancient DNA evidence for Old World origin of New World dogs. Science 298: 1613–1616. PubMed

Savolainen P, Zhang Y, Luo J, Lundeberg J, Leitner T (2002) Genetic evidence for an east Asian origin of domestic dogs. Science 298: , 1610–1613. PubMed

Gundry RL, Allard MW, Moretti TR, Honeycutt RL, Wilson MR, et al. (2007) Mitochondrial DNA analysis of the domestic dog: control region variation within and among breeds. J Forens Sci 52: 562–572. PubMed

Bannasch DL, Bannasch MJ, Ryun JR, Famula TR, Pedersen NC (2005) Y chromosome haplotype analysis in purebred dogs. Mamm Gen 16: 273–280. PubMed

Parker HG, Kim LV, Sutter NB, Carlson S, Lorentzen TD, et al. (2004) Genetic structure of the purebred domestic dog. Science 304: 1160–1164. PubMed

Irion DN, Schaffer AL, Famula TR, Eggleston ML, Hughes SS, et al. (2003) Analysis of genetic variation in 28 dog breed populations with 100 microsatellite markers. J Hered 94: 81–87. PubMed

vonHoldt BM, Pollinger JP, Lohmueller KE, Han E, Parker HG, et al. (2010) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464: 898–903. PubMed PMC

Řičánková V, Zrzavý J (2004) Phylogeny of Canidae (Mammalia) and evolution of reproductive, developmental and socio-ecological traits: inferences from morphological, behavioural and molecular data. Zool Scri 33: 311–333.

Bardeleben C, Moore RL, Wayne RK (2005) A molecular phylogeny of the Canidae based on six nuclear loci. Mol Phyl Evol 37: 815–831. PubMed

Pionnier-Capitan M, Bemilli C, Bodu P, Célérier G, Ferrié J-G, et al. (2011) New evidence for Upper Palaeolithic small domestic dogs in South-Western Europe. J Archaeol Sci 38: 2123–2140.

Morey DF (1994) The early evolution of the domestic dog. Am Sci 82: 336–347.

MacDonald DW, Sillero-Zubiri Z (2004) The biology and conservation of wild canids. Oxford University Press. 464 p.

Sundquist AK, Björnerfeldt K, Leonard JA, Hailer F, Hedhammar A, et al. (2006) Unequal contribution of sexes in the origin of dog breeds. Genetics 172: 1121–1128. PubMed PMC

Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34: 292–307. PubMed

Geffen E, Gompper ME, Gittleman JL, Hang-Kwang L, MacDonald DW, et al. (1996) Size, life-history traits, and social organization in the Canidae: A reevaluation. Am Nat 147: 140–160.

Kutzler MA, Yeager AE, Mohammed HO, Meyers-Wallen VN (2003) Accuracy of canine parturition date prediction using fetal measurements obtained by ultrasonography. Theriogenology 60: 1309–1317. PubMed

Stern DL, Orgogozo V (2009) Is genetic evolution predictable? Science 323: 746–751. PubMed PMC

Polák J, Frynta D (2010) Sexual size dimorphism in domestic cattle supports Rensch’s rule. Evol Ecol 24: 1255–1266.

Polák J, Frynta D (2009) Sexual size dimorphism in domestic goats, sheep and their wild relatives. Biol J Linn Soc 98: 872–883.

Lovich JE, Gibbons JW (1992) A review of techniques for quantifying sexual size dimorphism. Growth, Devel Aging 56: 269–281. PubMed

Smith RJ (1999) Statistics of sexual size dimorphism. J Hum Evol 36: 423–459. PubMed

McArdle BH (1988) The structural relationship: regression in biology. Can J Zool 66: 2329–2339.

StatSoft Inc. (accessed 2001) STATISTICA, Version 6.0. http://www.statsoft.com.

Strong support for Rensch's rule in an American clade of lizards (Teiidae and Gymnophtalmidae) and a paradox of the largest tejus

Sexual size dimorphism in ground squirrels (Rodentia: Sciuridae: Marmotini) does not correlate with body size and sociality