Cats and dogs cross the line: domestic breeds follow Rensch’s rule, their wild relatives do not

The domestication syndrome already recognized by Darwin shows that domesticated species acquire a number of novel morphological, physiological and behavioral characteristics not present in their wild ancestors. Because body size and sexual size dimorphism (SSD) are essential characteristics of species that affect most aspects of their life histories, we studied the effects of domestication on body size and SSD in domestic dogs and cats in comparison with their wild relatives: the Canidae and Felidae, respectively, and also analyzed the occurrence of Rensch’s rule within both domestic species. We studied maximum body mass and maximum height at withers of 64 and 89 domestic dog breeds respectively, and maximum body mass of 37 domestic cat breeds as well as body mass data for 36 wild Canidae and 36 wild Felidae from our previous studies. Our results have shown that domestic dogs maintain a level and range of body mass which largely exceeds that of the Canidae as a whole while maintaining a similar degree and range of SSD. On the contrary, domestic cats show a much reduced body mass range within the limits of their ancestor species while showing comparable levels of SSD as shown by the Felidae. Regarding Rensch’s rule, both Reduced Major Axis and Ordinary Least Squares regressions showed that both domestic species present a scaling of male and female body sizes consistent with Rensch’s rule while their wild relatives do not. We discuss these findings in the light of present knowledge about the domestication of Canis familiaris and Felis catus.

1. Abouheif E., Fairbairn D.J. A comparative analysis of sexual size dimorphism: assessing Rensch’s rule. Am. Naturalist. 1997;149:540-562.

2. Andersen N.M. The evolution of sexual size dimorphism and mating systems in water striders (Hemiptera: Gerridae): a phylogenetic approach. Ecoscience. 1994;1:208-214.

3. Andersson M. Sexual Selection. Princeton, N. J., 1994.

4. Asa C.S., Valdespino C. Canid reproductive biology: an integration of proximate mechanisms and ultimate causes. Am. Zoologist. 1998; 38:251-259.

5. Belyaev D.K. Destabilizing selection as a factor in domestication. J. Heredity. 1979;70:301-308.

6. Belyaev D.K., Trut L.N. Accelerating evolution. Science in the USSR. 1982;5:24-29.

7. Bell J.S., Cavanagh K.E., Tilley L.P., Smith F.W.K. Veterinary Medical Guide to Dog and Cat Breeds. Jackson W. Y., 2012.

8. Bidau C.J. Domestication through the centuries: Darwin’s ideas and Dmitry Belyaev’s long- term experiment in silver foxes. Gayana. 2009;73(1):55-72. DOI 10.4067/S0717-65382009000300006.

9. Bidau C.J. Some historical aspects of ecogeographic rules: Bergmann’s rule as an emblematic case. Entomol. Ornithol. Herpetol. 2014;2(3): 1-10.

10. Bidau C.J., Marti D.A. Contrasting patterns of sexual size dimorphism in the grashoppers Dichroplus vittatus and D. pratensis (Acrididae, Melanoplinae). J. Orthoptera Res. 2008a;17:201-211.

11. Bidau C.J., Marti D.A. Rensch’s rule in Dichroplus pratensis: a reply to Wolak. Ann. Entomol. Soc. Am. 2008b;101:802-803.

12. Bidau C.J., Martinez P.A. Sexual size dimorphism and Rensch’s rule in Canidae. Biol. J. Linn. Soc. 2016;119:816-830. DOI 10.1111/Bij.12848.

13. Bidau C.J., Taffarel A., Castillo E.R. Breaking the rule: multiple patterns of scaling of sexual size dimorphism with body size in orthopteroid insects. Revista de la Sociedad Entomológica Argentina. 2016;75:11-36.

14. Blanckenhorn W.U. Behavioral causes and consequences of sexual size dimorphism. Ethology. 2005;111:977-1016.

15. Blanckenhorn W.U., Stillwell R.C., Young K.A., Fox C.W., Ashton K.G. When Rensch meets Bergmann: does sexual size dimorphism change systematically with latitude? Evolution. 2006;60:2004-2011.

16. Calder W.A. III. Size, Function, and Life History. Cambridge, MA: Harvard Univ. Press, 1984.

17. Clutton-Brock J. Animals as Domesticates: A World View through History. East Lansing, 2012.

18. Collen B., Purvis A., Gittleman J.L. Biological correlates of description date in carnivores and primates. Global Ecol. Biogeogr. 2004;13:459-467.

19. Cox R.M., Butler M.A., John-Alder H.B. The evolution of sexual size dimorphism in reptiles. Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Eds. D.J. Fairbairn, W.U. Blanckenhorn, T. Székely, Oxford, 2007;38-49.

20. Dale J., Dunn P.O., Figuerola J., Lislevand T., Székely T., Wittingham L.A. Sexual selection explains Rensch’s rule of allometry for sexual size dimorphism. Proc. R. Soc. B. 2007;274:2971-2979.

21. Daniels T.J. The social organization of free-ranging urban dogs. II. Estrous groups and the mating system. Appl. Anim. Ethol. 1983;10: 365-373.

22. Darwin C. On the Origin of Species by Means of Natural Selection. 1st Edit. London, 1859.

23. Darwin C. The variation of animals and plants under domestication. London, 1868;I;II.

24. Darwin C. The Descent of Man and Selection in Relation to Sex. London, 1871;I;II.

25. Driscoll C.A., Menotti-Raymond M., Roca A.L., Karsten H., Johnson W.E., Geffen E., Harley E.H., Delibes M., Pontier D., Kitchener A.C., Yamaguchi N., O’Brien S.J., Macdonald D.W. The Near Eastern origin of cat domestication. Science. 2007;317:519-523.

26. Fairbairn D.J. 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.

27. Fairbairn D.J. Allometry for sexual size dimorphism: testing two hypotheses for Rensch’s rule in the water strider Aquarius remigis. Am. Naturalist. 2005;66:S69-S84.

28. Fairbairn D.J. Introduction: the enigma of sexual size dimorphism. Evolutionary Studies of Sexual Size Dimorphism: Sex, Size and Gender Roles. Eds. D.J. Fairbairn, W.U. Blanckenhorn, T. Székely. Oxford, 2007;1-12.

29. Fairbairn D.J. Odd Couples: Extraordinary Differences between the Sexes in the Animal Kingdom. Oxford, 2013.

30. Fairbairn D.J., Blanckenhorn W.U., Székely T. (Eds.) Sex, Size and Gender Roles. Evolutionary Studies of Sexual Size Dimorphism. Oxford, 2007.

31. Frynta D., Baudyšová J., Hradcová P., Faltusová K., Kratochvíl L. Allometry of sexual size dimorphism in domestic dog. PLoS ONE. 2012;7(9):e46125. DOI 10.1371/journal.pone.0046125.

32. Galis F., Van Der Sluijs I., Van Dooren T.J.M., Metz J.A.J., Nussbaumer M. Do large dogs die young? J. Exp. Zool. (Mol. Dev. Evol.). 2007;308B:119-126. DOI 10.1002/jez.b. 21116.

33. Greer K.A., Canterberry S.C., Murphy K.E. Statistical analysis regarding the effects of height and weight on life span of the domestic dog. Res. Vet. Sci. 2007;82:208-214. DOI 10.1016/j.rvsc.2006.06.005.

34. Hart B.L., Hart L.A. Normal and problematic reproductive behaviour in the domestic cat. The Domestic Cat. The Biology of its Behaviour. 3rd Edit. Eds. D.C. Turner, P. Bateson. Cambridge, UK, 2014;27-36.

35. Hu Y., Hu S., Wang W., Wu X., Marshall F.B., Chen X., Wang C. Earliest evidence for commensal processes of cat domestication. Proc. Natl. Acad. Sci. USA. 2014;111:116-120. DOI/10.1073/pnas.1311439110.

36. Isaac J.L. Potential causes and life-history consequences of sexual size dimorphism in mammals. Mamm. Rev. 2005;35:101-115.

37. Lande R. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution. 1980;34:292-305.

38. Lark K.G., Chase K., Sutter N.B. Genetic architecture of the dog: sexual size dimorphism and functional morphology. Trends Genet. 2006; 22:537-544. DOI 10.1016/j.tig.2006.08.009.

39. Larson G., Fuller D.Q. The evolution of animal domestication. Annu. Rev. Ecol. Evol. Syst. 2014;45:115-136. DOI 10.1146/annurev-ecolsys-110512-135813.

40. Larson G., Karlsson E.K., Perri A., Webster M.T., Ho S.Y.W, Peters J., Stahl P.W., Piper P.J.,

41. Lingaas F., Fredholm M., Comstock K.E., Modiano J.F., Schelling C., Agoulnik A.I., Leegwater P.A., Dobney K., Vignes J.-D., Vilà C., Andersson L., Lindblad-Toh K. Rethinking dog domestication by integrating genetics, archeology, and biogeography. Proc. Natl. Acad. Sci. USA. 2012;109:8878-8883. DOI 10.1073/pnas.1203005109.

42. Legendre P. Package ‘lmodel2’ for R. http://cran.r-project.org/web/packages/Imodel2.pdf. 2015.

43. Liao W.B., Zeng Y., Zhou C.Q., Jehle R. Sexual size dimorphism in anurans fails to obey Rensch’s rule. Front. Zool. 2013;10:10. DOI 10.1186/1742-9994-10-10.

44. Liberg O., Sandell M., Pontier D., Natoli E. Density, spatial organisation and reproductive tactics in the domestic cat and other felids. The Domestic Cat: The Biology of its Behaviour. 2nd Edit. Eds. D.C. Turner, P. Bateson. Cambridge, UK: Cambr. Univ. Press, 2000;119-147.

45. Lindenfors P., Gittleman J.L., Jones K.E. Sexual size dimorphism in mammals. Sex, Size and Gender Roles. Evolutionary Studies of Sexual Size Dimorphism. Eds. D.J. Fairbairn, W.U. Blanckenhorn, T. Székely. Oxford, 2007;16-26.

46. Lindenfors P., Tullberg B.S, Biuw M. Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds. Behav. Ecol. Sociobiol. 2002;52:188-193.

47. Lord K., Feinstein M., Smith B., Coppinger R. Variation in reproductive traits of members of the genus Canis with special attention to the domestic dog (Canis familiaris). Behav. Proc. 2013;92:131-142.

48. 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. 2016;81:66-72. DOI 10.1016/j.mambio.2014.11.008.

49. Martínez P.A., Amado T.F., Bidau C.J. A phylogenetic approach to the study of sexual size dimorphism in Felidae and an assessment of Rensch’s rule. Ecosistemas. 2014;23:27-36.

50. Meiri S., Kadison A.E., Novosolov M., Pafilis P., Foufopoulos J., Itescu Y., Pincheira-Donoso D. The number of competitor species is unlinked to sexual dimorphism. J. Anim. Ecol. 2014;83:1302-1312.

51. O’Neill D.G., Church D.B., McGreevy P.D., Thomson P.C., Brodbelt D.C. Longevity and mortality of cats attending primary care veterinary practices in England. J. Feline Med. Surg. 2015;17:125- 133. DOI 1098612X14536176.

52. Perri A. A wolf in dog’s clothing: Initial dog domestication and Pleistocene wolf variation. J. Archaeol. Sci. 2016;68:1-4. DOI 10.1016/j.jas.2016.02.003.

53. Peters R. The ecological implications of body size. Cambridge, UK, 1983.

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

55. Polák J., Frynta D. Patterns of sexual size dimorphism in cattle breeds support Rensch’s rule. Evol. Ecol. 2010;24:1255-1266. DOI 10.1007/s10682-010-9354-9.

56. Pontier D., Fromont E., Courchamp F., Artois M., Yoccoz N.G. Retroviruses and sexual size dimorphism in domestic cats (Felis catus L.). Proc. R. Soc. B. 1998; 265:167-173.

57. Ranta E., Laurila A., Elmberg J. Reinventing the wheel: analysis of sexual dimorphism in body size. Oikos. 1994;70(3):313-321.

58. Reiss M.J. Sexual dimorphism in body size: are larger species more dimorphic? J. Theor. Biol. 1986;121:163-172.

59. Reiss M.J. The Allometry of Growth and Reproduction. Cambridge, UK, 1989.

60. Remeš V., Székely T. Domestic chickens defy Rensch’s rule: sexual size dimorphism in chicken breeds. J. Evol. Biol. 2010;23:2754-2759. DOI 10.1111/j.1420-9101.2010.02126.x.

61. Rensch B. Die Abhangigkeit der Relativen Sexual differenz von der Korpergrosse. Bonner Zoologische Beiträge. 1950;1:58-69.

62. Rensch B. Evolution above the Species Level. N. Y., 1960.

63. Ruckstuhl K.E., Neuhaus P. (Eds.) Sexual Segregation in Vertebrates: Ecology of the Two Sexes. Cambridge, UK, 2005.

64. Sánchez-Villagra M.R., Geiger M., Schneider R.A. The taming of the neural crest: a developmental perspective on the origins of morphological covariation in domesticated mammals. R. Soc. Open Sci. 2016;3:160107. DOI 10.1098/rsos.160107.

65. Schmidt-Nielsen K. Scaling: Why is Animal Size so Important? Cambridge, UK, 1984.

66. Serpell J.A. Domestication and history of the cat. The Domestic Cat: The Biology of its Behavior. 3rd Edit. Eds. D.C. Turner, P. Bateson, Cambridge, UK, 2014;83-100.

67. Sibly R.M., Zuo W., Kodric-Brown A., Brown J.H. Rensch’s rule in large herbivorous mammals derived from metabolic scaling. Am. Naturalist. 2012;179:169-177. DOI 10.5061/dryad.17vs2d34.

68. Simpson L.A., Ambrosio L.J., Baeza J.A. Sexual dimorphism and allometric growth in the enigmatic pygmy crab Petramithrax pygmaeus (Bell, 1836) (Decapoda: Brachyura: Mithracidae), with a formal test of Rensch’s rule in spider crabs (superfamily Majoidea). J. Crustacean Biol. 2016;36:792-803. DOI 10.1163/1937240x-00002486.

69. Skoglund P., Ersmark E., Palkopoulou E., Dalén L. Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds. Curr. Biol. 2015;25:1515-1519. DOI 10.1016/j.cub.2015.04.019.

70. Smith R.J., Cheverud J.M. Scaling of sexual dimorphism in body mass: a phylogenetic analysis of Rensch’s rule in Primates. Int. J. Primatol. 2002;23:1095-1135.

71. Stevens R.D., Platt R.N. Patterns of secondary sexual size dimorphism in new world Myotis and a test of Rensch’s rule. J. Mammalogy. 2015;96:1128-1134. DOI 10.1093/jmammal/gyv120.

72. Sutter N.B., Mosher D.S., Gray M.M., Ostrander E.A. Morphometrics within dog breeds are highly reproducible and dispute Rensch’s rule. Mamm. Genome. 2008;19:713-723. DOI 10.1007/s00335-008-9153-6.

73. Székely T., Lislevand T., Figuerola J. Sexual size dimorphism in birds. Sex, Size and Gender Roles. Evolutionary Studies of Sexual Size Dimorphism. Eds. D.J. Fairbairn, W.U. Blanckenhorn, T. Székely. Oxford, 2007;27-37.

74. Thalmann O., Shapiro B., Cui P., Schuenemann V.J., Sawyer S.K., Greenfield D.L., Germonpré M.B., Sablin M.V., López-Giráldez F., Dominog-Roura X., Napierala H., Uerpmann H.P., Loponte D.M., Acosta A.A., Giemsch L., Schmitz R.W., Worthington B., Buikstra J.E., Druzhkova A., Graphodatsky A.S., Ovodov N.D., Wahlberg N., Freedman A.H., Schweizer R.M., Koepfli K.P., Leonard J.A., Meyer M., Krause J., Pääbo S., Green R.E., Wayne R.K. Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs. Science. 2013;342:871-874. DOI 10.1016/j.jas.2016.02.003.

75. Torres-Romero E.J., Olalla-Tárraga M.A. Bergmann’s rule in the oceans? Temperature strongly correlate with global interspecific patterns of body size in marine mammals. Global Ecol. Biogeogr. 2016; 25:1206-1215.

76. Trut L. Early canid domestication: the farm-fox experiment. Am. Scientist. 1999;87:160-169.

77. Trut L.N., Markel A.L., Borodin P.M., Argutinskaya S.V., Zakharov I.K., Shumny V.K. To the 90th anniversary of Academician Dmitry Konstantinovich Belyaev (1917–1985). Russ. J. Genetics. 2007;43(7):717-720.

78. Tubaro P.L., 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.

79. Vigne J.D., Guilaine J., Debue K., Haye L., Gérard P. Early taming of the cat in Cyprus. Science. 2004;304:259-259.

80. Wallace A.R. Darwinism. London; New York, 1889.

81. Webb T.J., Freckleton R.P. Only half right: species with female-biased sexual size dimorphism consistently break Rensch’s rule. PLoS ONE. 2007;9:e897. DOI 10.1371/journal.pone.0000897.

82. Weckerly F.W. Sexual-size dimorphism: influence of mass and mating systems in the most dimorphic mammals. J. Mammalogy. 1998;79: 33-52.

83. Werner Y.L., Korolker N., Guy S. Bergmann’s and Rensch’s rules and the spur-thighed tortoise (Testudo graeca). Biol. J. Linn. Soc. 2016; 117:796-811. DOI 10.1111/bij.12717.

84. Wilkins A.S., Wrangham R.W., Fitch W.T. The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics. 2014;197:795-808. DOI 10.1534/genetics.114.165423.

85. Wu H., Jiang T., Huang X., Lin H., Wang H., Wang L., Niu H., Feng J. A test of Rensch’s rule in Greater Horseshoe Bat (Rhinolophus ferrumequinum) with female-biased sexual size dimorphism. PLoS ONE. 2014;9(1):e86085. DOI 10.1371/journal.pone.0086085.

86. Zeder M.A. The domestication of animals. J. Anthropol. Res. 2012;68: 161-190.

87. Zeder M.A. Core questions in domestication research. Proc. Natl. Acad. Sci. USA. 2015;112:3191-3198. DOI 10.1073/pnas.1501711112.