Skip to main content Accessibility help

The evolution of heterochiasmy: the role of sexual selection and sperm competition in determining sex-specific recombination rates in eutherian mammals

  • JUDITH E. MANK (a1)


Early karyotypic work revealed that female and male recombination rates in many species show pronounced differences, and this pattern of heterochiasmy has also been observed in modern linkage mapping studies. Several hypotheses to explain this phenomenon have been offered, ranging from strictly biological mechanisms related to the gametic differences between the sexes, to more evolutionary models based on sexually antagonistic selection. However, despite the long history of interest in heterochiasmy, empirical data has failed to support any theory or pattern consistently. Here I test two alternative evolutionary hypotheses regarding heterochiasmy across the eutherian mammals, and show that sexual dimorphism, but not sperm competition, is strongly correlated with recombination rate, suggesting that sexual antagonism is an important influence. However, the observed relationship between heterochiasmy and sexual dimorphism runs counter to theoretical predictions, with male recombination higher in species with high levels of sexual dimorphism. This may be the response to male-biased dispersal, which, rather than the static male fitness landscape envisioned in the models tested here, could radically shift optimal male fitness parameters among generations.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      The evolution of heterochiasmy: the role of sexual selection and sperm competition in determining sex-specific recombination rates in eutherian mammals
      Available formats

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      The evolution of heterochiasmy: the role of sexual selection and sperm competition in determining sex-specific recombination rates in eutherian mammals
      Available formats

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      The evolution of heterochiasmy: the role of sexual selection and sperm competition in determining sex-specific recombination rates in eutherian mammals
      Available formats


Corresponding author

*Corresponding author. E-mail:


Hide All
Aguade, M. (1999). Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila. Genetics 152, 543551.
Åkesson, M., Hansson, B., Hasselquist, D. & Bensch, S. (2007). Linkage mapping of AFLP markers in a wild population of great reed warblers: importance of heterozygosity and number of genotyped individuals. Molecular Ecology 16, 21892202.
Anderson, K. G. (2006). How well does paternity confidence match actual paternity? Current Anthropology 47, 513520.
Archibald, A. L., Haley, C. S., Brown, J. F., Couperwhite, S., McQueen, H. A., Nicholson, D., Coppieters, W., Vandeweghe, A., Stratil, A., Wintero, A. K., Fredholm, M., Larsen, N. J., Nielsen, V. H., Milan, D., Woloszyn, N., Robic, A., Dalens, M., Riquet, J., Gellin, J., Caritez, J. C., Burgaud, G., Ollivier, L., Bidanel, J. P., Vaiman, M., Renard, C., Geldermann, H., Davoli, R., Ruyter, D., Verstege, E. J. M., Groenen, M. A. M., Davies, W., Hoyheim, B., Keiserud, A., Andersson, L., Ellegren, H., Johansson, M., Marklund, L., Miller, J. R., Dear, D. V. A., Signer, E., Jeffreys, A. J., Moran, C., Letissier, P., Muladno, Rothschild M. F., Tuggle, C. K., Vaske, D., Helm, J., Liu, H. C., Rahman, A., Yu, T. P., Larson, R. G. & Schmitz, C. B. (1995). The PigMap consortium linkage map of the pig (Sus Scrofa). Mammalian Genome 6, 157175.
Arnason, U., Adegoke, J. A., Gullberg, A., Harley, E. H., Janke, A. & Kullberg, M. (2008). Mitogenomic relationships of placental mammals and molecular estimates of their divergences. Gene 421, 3751.
Begun, D. J. & Lindfors, H. A. (2005). Rapid Evolution of Genomic Acp complement in the melanogaster subgroup of Drosophila. Molecular Biology and Evolution 22, 20102021.
Bercovitch, F. B. & Nurnberg, P. (1997). Genetic determination of paternity and variation in male reproductive success in two populations of rhesus macaques. Electrophoresis 18, 17011705.
Bradshaw, J. & Cameron-Beaumont, C. (2000). The signalling repertoire of the domestic cat and its undomesticated relatives. In The Domestic Cat: The Biology of its Behaviour, pp. 6794. Cambridge: Cambridge University Press.
Broman, K. W., Murray, J. C., Sheffield, V. C., White, R. L. & Weber, J. L. (1998). Comprehensive human genetic maps: Individual and sex-specific variation in recombination. American Journal of Human Genetics 63, 861869.
Burt, A., Bell, G. & Harvey, P. H. (1991). Sex differences in recombination. Journal of Evolutionary Biology 4, 259277.
Chakravarti, A., Lasher, L. K. & Reefer, J. E. (1991). A maximum likleihood method for estimating genome length using genetic linkage data. Genetics 128, 175182.
Charlesworth, B. (1976). Recombination modification in a fluctuatung evironment. Genetics 83, 181195.
Coltman, D. W., Bancroft, D. R., Robertson, A., Smith, J. A., Clutton-Brock, T. H. & Pemberton, J. M. (1999). Male reproductive success in a promiscuous mammal: behvaioural estimates compared with genetic paternity. Molecular Ecology 8, 11991209.
Cox, L. A., Mahaney, M. C., VandeBerg, J. L. & Rogers, J. (2006). A second-generation genetic linkage map of the baboon (Papio hamadryas) genome. Genomics 88, 274281.
de Villena, F. P. M. & Sapienza, C. (2001). Recombination is proportional to the number of chromosome arms in mammals. Mammalian Genome 12, 318322.
Dean, M. D., Ardlie, G. & Nachman, M. W. (2006). The frequency of multiple paternity suggests sperm competition is common in house mouse. Molecular Ecology 15, 41414151.
Delgado, R., Fernandez-Llario, P., Azevedo, M., Beja-Pereira, A. & Santos, P. (2008). Paternity assessment in free-ranging wild boar (Sus scrofa) – Are littermates full-sibs? Mammalian Biology 73, 169176.
Drogemuller, C., Karlsson, E. K., Hytonen, M. K., Perloski, M., Dolf, G., Sainio, K., Lohi, H., Lindblad-Toh, K. & Leeb, T. (2008). A mutation in hairless dogs implicates FOXI3 in ectodermal development. Science 321, 14621462.
Dumont, B. L. & Payseur, B. A. (2007). Evolution of the genomic rate of recombination in mammals. Evolution 62, 276294.
Felsenstein, J. & Yokoyama, S. (1976). Evolutionary advantage of recombination. II. Individual selection for recombination. Genetics 83, 845859.
Gates, C. C. & Larter, N. C. (1990). Growth and dispersal of an erupting large herbivore population in northern Canada: The Mackenzie wood bison. Arctic 43, 231238.
Haldane, J. (1922). Sex ratio and unisexual sterility in hybrid animals. Journal of Genetics 12, 101109.
Hall, M. C. & Willis, J. H. (2005). Transmission ratio distortion in intraspecific hybrids of Mimulus gutatus: implications for genomic divergence. Genetics 170, 375386.
Hansson, B., Åkesson, M., Slate, J. & Pemberton, J. M. (2005). Linkage mapping reveals sex-dimorphic map distances in a passerine bird. Proceedings of the Royal Society B-Biological Sciences 272, 22892298.
Hellmann, I., Ebersberger, I., Ptak, S. E., Pääbo, S. & Przeworski, M. (2003). A neutral explanation for the correlation of diversity with recombination rates in humans. American Journal of Human Genetics 72, 15271535.
Hernandez, R. D., Hubisz, M. J., Wheeler, D. A., Smith, D. G., Ferguson, B., Rogers, J., Nazareth, L., Indap, A., Bourquin, T., McPherson, J., Muzny, D., Gibbs, R., Nielsen, R. & Bustamante, C. D. (2007). Demographic histories and patterns of linkage disequilibrium in Chinese and Indian rhesus macaques. Science 316, 240243.
Huxley, J. (1928). Sexual differences in linkage in Gammarus chevruxi. Journal of Genetics 20, 145156.
Ihara, N., Takasuga, A., Mizoshita, K., Takeda, H., Sugimoto, M., Mizoguchi, Y., Hirano, T., Itoh, T., Watanabe, T., Reed, K. M., Snelling, W. M., Kappes, S. M., Beattie, C. W., Bennett, G. L. & Sugimoto, Y. (2004). A comprehensive genetic map of the cattle genome based on 3802 microsatellites. Genome Research 14, 19871998.
Karlsson, E. K. & Lindblad-Toh, K. (2008). Leader of the pack: gene mapping in dogs and other model organisms. Nature Reviews Genetics 9, 713725.
Kruuk, L. E. B., Slate, J., Pemberton, J. M., Brotherstone, S., Guinness, F. & Clutton-Brock, T. (2002). Antler size in red deer: Heritability and selection but no evolution. Evolution 56, 16831695.
Lee, S., Blay, S., Mooers, A. O., Singh, A. & Oakley, T. H. (2006). CoMET: A Mesquite package for comparing models of continuous character evolution on phylogenies. Evolutionary Bioinformatics Online 2, 193196.
Lenormand, T. & Dutheil, J. (2005). Recombination difference between sexes: A role for haploid selection. Plos Biology 3, 396403.
Lenormand, T. & Otto, S. P. (2000). The evolution of recombination in a heterogeneous environment. Genetics 156, 423428.
Lercher, M. J., Hurst, L. D. (2002). Human SNP variability and mutation rate are higher in regions of high recombination. Trends in Genetics 18, 337340.
Maddison, W. P. & Maddison, D. R. (2009). Mesquite: a modular system for evolutionary analysis. 2.6 ed.
Maddox, J. F., Davies, K. P., Crawford, A. M., Hulme, D. J., Vaiman, D., Cribiu, E. P., Freking, B. A., Beh, K. J., Cockett, N. E., Kang, N., Riffkin, C. D., Drinkwater, R., Moore, S. S., Dodds, K. G., Lumsden, J. M., van Stijn, T. C., Phua, S. H., Adelson, D. L., Burkin, H. R., Broom, J. E., Buitkamp, J., Cambridge, L., Cushwa, W. T., Gerard, E., Galloway, S. M., Harrison, B., Hawken, R. J., Hiendleder, S., Henry, H. M., Medrano, J. F., Paterson, K. A., Schibler, L., Stone, R. T. & van Hest, B. (2001). An enhanced linkage map of the sheep genome comprising more than 1000 loci. Genome Research 11, 12751289.
Maestripieri, D., Mayhew, J., Carlson, C. L., Hoffman, C. L. & Radtke, J. M. (2007). One-male harems and female social dynamics in Guinea baboons. Folia Primatologica 78, 5668.
McVean, A. T., Myers, S. R., Hunt, S., Deloukas, P., Bentley, D. R. & Donnelly, P. (2004). The fine-scale structure of recombination rate variation in the human genome. Science 304, 581584.
Meiklejohn, C. D., Parsch, J., Ranz, J. M. & Hartl, D. L. (2003). Rapid evolution of male-biased gene expression in Drosophila. Proceedings of the National Academy of Sciences, USA 100, 98949899.
Menotti-Raymond, M., David, V. A., Schaffer, A. A., Tomlin, J. F., Eizirik, E., Phillip, C., Wells, D., Pontius, J. U., Hannah, S. S. & O'Brien, S. J. (2009). An autosomal genetic linkage map of the domestic cat, Felis sylvestris catus. Genomics 93, 305313.
Neff, M. W., Broman, K. W., Mellersh, C. S., Ray, K., Acland, G. M., Aguirre, G. D., Ziegle, J. S., Ostrander, E. A. & Rine, J. (1999). A second-generation genetic linkage map of the domestic dog, Canis familiaris. Genetics 151, 803820.
Norris, K. (1993). Heritable variation in a plumage indicator of variability in male great tits - Parus major. Nature 362, 537539.
Nowak, R. M. (1999). Walker's Mammals of the World. Baltimore, MD: Johns Hopkins University Press.
Otto, S. P. & Barton, N. H. (2001). Selection for recombination in small populations. Evolution 55, 19211931.
Otto, S. P. & Nuismer, S. L. (2004). Species interactions and the evolution of sex. Science 304, 10181020.
Pagel, M. (1994). Detecting correlated evolution on phylogenies, a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London, B 255, 3745.
Pal, S. K., Ghosh, B. & Roy, S. (1998). Dispersal behaviour of free-ranging dogs (Canis familiaris) in relation to age, sex, season, and dispersal distance. Applied Animal Behaviour Science 61, 123132.
Perry, P. E. & Jones, G. H. (1974). Male and female meiosis in grasshoppers. I. Stethophyma grossum. Chromosoma 47, 227236.
Prasad, A. B., Allard, M. W., Green, E. D. & Program, N. C. S. (2008). Confirming the phylogeny of mammals by use of large comparative sequence data sets. Molecular Biology and Evolution 25, 17951808.
Pusey, A. E. & Packer, C. (1986). Dispersal and Philopatry. Chicago: Primate societies. University of Chicago Press.
Reynolds, J. D. & Gross, M. R. (1990). Costs and benefits of female mate choice - is there a lek paradox. American Naturalist 136, 230243.
Ritchie, M. G. (1996). The shape of female mating preferences. Proceedings of the National Academy of Sciences, USA 93, 1462814631.
Roden, C., Vervaecke, H., Mommens, G. & van Elsacker, L. (2003). Reproductive success of bison bulls (Bison bison) in semi-natural conditions. Animal Reproductive Science 79, 3343.
Rogers, J., Mahaney, M. C., Witte, S. M., Nair, S., Newman, D., Wedel, S., Rodriguez, L. A., Rice, K. S., Slifer, S. H., Perelygin, A., Slifer, M., Palladino-Negro, P., Newman, T., Chambers, K., Joslyn, G., Parry, P. & Morin, P. A. (2000). A genetic linkage map of the baboon (Papio hamadryas) genome based on human microsatellite polymorphisms. Genomics 67, 237247.
Rogers, J., Garcia, R., Shelledy, W., Kaplan, J., Arya, A., Johnson, Z., Bergstrom, M., Novakowski, L., Nair, P., Vinson, A., Newman, D., Heckman, G. & Cameron, J. (2006). An initial genetic linkage map of the rhesus macaque (Macaca mulatta) genome using human microsatellite loci. Genomics 87, 3038.
Samollow, P. B., Kammerer, C. M., Mahaney, S. M., Schneider, J. L., Westenberger, S. J., VendeBerg, J. L. & Robinson, E. S. (2004). First-generation linkage map of the gray, short-tailed opossum, Monodelphis domestica, reveals genome-wide reduction in female recombination rates. Genetics 166, 307329.
Schnabel, R. D., Taylor, J. F. & Derrm, J. N. (2003). Development of a linkage map and QTL scan for growth traits in North American bison. Cytogenetic and Genome Research 102, 5964.
Shifman, S., Bell, J. T., Copley, R. R., Taylor, M. S., Williams, R. W., Mott, R. & Flint, J. (2006). A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biology 4, 22272237.
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.
Thomson, P. C., Rose, K. & Kok, N. E. (1992). The behavioural ecology of dingoes in northwestern Australia. VI. Temporary extraterritorial movements and dispersal. Wildlife Research 19, 585595.
Trivers, R. (1988). Sex differences in rates of recombination and sexual selection. In The Evolution of Sex (ed. Michod, R. & Levin, B. R.), pp. 270286. Sunderland, MA: Sinauer Press.
Truve, J. & Lemel, J. (2003). Timing and distance of natal dispersal for wild boar Sus scrofa in Sweden. Wildlife Biology 9, 5157.
Turner, D. C. & Bateson, P. (2000). The domestic cat: the biology of its behaviour. Cambridge: Cambridge University Press.
Van Vuure, C. (2005). Retracing the aurochs: History, morphology and ecology of an extinct wild ox. Sofia: Pensoft.
Wedell, N. & Tregenza, T. (1990). Successful fathers sire successful sons. Evolution 53, 620625.
Widdig, A., Bercovitch, F. B., Streich, W. J., Sauermann, U., Nurnberg, P. & Krawczak, M. (2004). A longitudinal analysis of reproductive skew in male rhesus macaques. Proceedings of the Royal Society, B 271, 819826.
Wiik, A. C., Wade, C., Biagi, T., Ropstad, E. O., Bjerkas, E., Lindblad-Toh, K. & Lingaas, F. (2008). A deletion in nephronophthisis 4 (NPHP4) is associated with recessive cone-rod dystrophy in standard wire-haired dachshund. Genome Research 18, 14151421.
Winckler, W., Myers, S. R., Richter, D. J., Onofrio, R. C., McDonald, G. J., Bontrop, R. E., McVean, G. A. T., Gabriel, S. B., Reich, D., Donnelly, P. & Altshuler, D. (2005). Comparison of fine-scale recombination rates in humans and chimpanzees. Science 308, 107111.
Woodall, P. F., Pavlo, P. & Tolley, L. K. (1993). Comparative dimensions of testes, epididymides and spermatozoa of Australian dingoes (Canis familiaris dingo) and domestic dogs (Canis familiaris familiaris): Some effects of domestication. Australian Journal of Zoology 41, 133140.
Zenger, K. R., McKenzie, L. M. & Coop, D. W. (2002). The first comprehensive linkage map of a marsupial: The tammar wallaby (Macropus eugenii). Genetics 162, 321330.
Zhang, Z. & Parsch, J. (2005). Positive correlation between evolutionary rate and recombination rate in Drosophila genes with male-biased expression. Molecular Biology and Evolution 22, 19451947.


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed