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Assortative Mating in Animals. Author(S): Yuexin Jiang, Daniel I The University of Chicago Assortative Mating in Animals. Author(s): Yuexin Jiang, Daniel I. Bolnick, and Mark Kirkpatrick Source: The American Naturalist, Vol. 181, No. 6 (June 2013), pp. E125-E138 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/670160 . Accessed: 11/05/2015 17:41 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org This content downloaded from 128.83.205.78 on Mon, 11 May 2015 17:41:51 PM All use subject to JSTOR Terms and Conditions vol. 181, no. 6 the american naturalist june 2013 E-Article Assortative Mating in Animals Yuexin Jiang,1,* Daniel I. Bolnick,2 and Mark Kirkpatrick1 1. Section of Integrative Biology, University of Texas, Austin, Texas 78712; 2. Howard Hughes Medical Institute and Section of Integrative Biology, University of Texas, Austin, Texas 78712 Submitted June 2, 2012; Accepted January 7, 2013; Electronically published April 26, 2013 Online enhancement: appendixes. Dryad data: http://dx.doi.org/10.5061/dryad.r706v. garding its behavioral mechanism or evolutionary role abstract: Assortative mating occurs when there is a correlation (Lewontin et al. 1968; Kondrashov and Shpak 1998). (positive or negative) between male and female phenotypes or ge- notypes across mated pairs. To determine the typical strength and Adopting this general view, assortative mating can be mea- direction of assortative mating in animals, we carried out a meta- sured as a correlation between the values of a homologous analysis of published measures of assortative mating for a variety of phenotypic or genotypic trait across members of mated phenotypic and genotypic traits in a diverse set of animal taxa. We pairs (Wright 1921; Lipsey and Wilson 2001; Redden and focused on the strength of assortment within populations, excluding Allison 2006). Assortative mating may be either positive, reproductively isolated populations and species. We collected 1,116 implying a tendency to mate with phenotypically similar published correlations between mated pairs from 254 species (360 individuals, or negative (also called disassortative), imply- unique species-trait combinations) in five phyla. The mean corre- lation between mates was 0.28, showing an overall tendency toward ing the converse (Partridge 1983; Hooper and Miller positive assortative mating within populations. Although 19% of the 2008). There are many empirical examples of both positive correlations were negative, simulations suggest that these could rep- and negative assortative mating (Johnston and Johnson resent type I error and that negative assortative mating may be rare. 1989; Follett et al. 2007; Pryke and Griffth 2007; Lu et al. We also find significant differences in the strength of assortment 2009), but it remains unclear what the distribution of the among major taxonomic groups and among trait categories. We dis- strength of assortative mating is in nature, especially cuss various possible reasons for the evolution of assortative mating whether there is a systematic tendency toward assortment, and its implications for speciation. random mating, or disassortment. Keywords: disassortative mating, distribution of assortment strength, Assortative mating has several important evolutionary mate choice, meta-analysis, nonrandom mating, sexual selection, consequences. Positive assortment increases homozygosity sympatric speciation. within loci, promotes linkage disequilibrium between loci, and consequently inflates the variance of quantitative traits (Lynch and Walsh 1998). The resulting deviations from Introduction Hardy-Weinberg equilibrium can cause statistical biases in Assortative mating is used to describe a variety of patterns association mapping studies (Redden and Allison 2006) of nonrandom mating. In the speciation literature, assor- and estimates of quantitative genetic parameters (Gimel- tative mating is treated as a mechanism of premating re- farb 1986). Assortative mating also plays a key role in productive isolation between distinct species or divergent speciation, contributing to premating isolation between populations (Johannesson et al. 1995; Seehausen et al. phenotypically divergent populations (Felsenstein 1981; 1997; Coyne and Orr 2004). In the behavioral literature, Kondrashov and Shpak 1998; Coyne and Orr 2004; Bol- assortative mating has been used to describe a particular nick and Kirkpatrick 2012). In models of adaptive spe- form of mate choice in which individuals select mates on ciation, reproductive isolation via positive assortative mat- the basis of phenotypic similarity to themselves (Crespi ing evolves in response to disruptive selection (Kirkpatrick 1989; Harari et al. 1999; Shine et al. 2001). More generally, 2000; Dieckmann et al. 2004; Gavrilets 2004; Bank et al. assortative mating can be defined as a pattern of nonran- 2011). Assortment is hypothesized to reduce the produc- dom mating, without making specific assumptions re- tion of less fit phenotypically intermediate offspring. Con- versely, stabilizing selection favors the evolution of disas- * Corresponding author; e-mail: [email protected]. sortative mating, which reduces the production of less fit Am. Nat. 2013. Vol. 181, pp. E125–E138. ᭧ 2013 by The University of Chicago. phenotypic extremes (Kondrashov and Shpak 1998; Kirk- 0003-0147/2013/18106-53880$15.00. All rights reserved. patrick and Ravigne´ 2002). Disassortative mating also in- DOI: 10.1086/670160 creases heterozygosity, decreases inbreeding depression This content downloaded from 128.83.205.78 on Mon, 11 May 2015 17:41:51 PM All use subject to JSTOR Terms and Conditions E126 The American Naturalist (Waser 1993; Pusey and Wolf 1996), and can facilitate the Sadedin et al. 2009). The typical assumption is that pop- maintenance of sexually antagonistic variation (Arnqvist ulations initially exhibit random mating, but this may not 2011). Given these multifarious evolutionary effects of as- be empirically justified. Meta-analysis can determine the sortative mating, it would be valuable to know the dis- distribution of assortment within populations, which can tribution of its strength in natural populations, as well as be treated as a range of biologically realistic initial con- its evolutionary origins. ditions in future models. Two general hypotheses could explain the occurrence Despite these needs for an overview of the strength and of assortative mating. The first asserts that the strength of direction of assortative mating, no comprehensive review assortative mating evolves adaptively in response to direct currently exists. Many studies focus on a single species or or indirect selection on mating preferences. Selection can clade and are typically based on a single phenotypic trait act directly on mate choice if fitness depends on the sim- (Olson et al. 1986; Arnqvist et al. 1996; Bernstein and ilarity of mated pairs. For example, conjugation in the Bernstein 2003; Ce´zilly 2004; Roulin 2004; Wogel et al. marine nudibranch Chromodoris zebra is facilitated when 2005). It is therefore unclear what general patterns might the partners are of similar size (Crozier 1917, 1918). Al- exist regarding the strength of assortative mating in animal ternatively, assortative mating can affect the fitness of a populations. Outstanding questions include the following: pair’s offspring, resulting in indirect selection on the par- What is the distribution of the strength of assortative mat- ents’ mating behavior. For example, Heliconius butterflies ing? How frequent is negative versus positive assortative that mate assortatively on the basis of mimetic color pat- mating? Are there differences in the strengths of assort- terns avoid producing offspring with maladaptive patterns ment among taxa and among different kinds of phenotypic (Chamberlain et al. 2009). More generally, disruptive se- traits? Are the data consistent with the hypothesis that lection will indirectly favor the evolution of positive as- assortment evolves adaptively in response to indirect ef- sortative mating to avoid producing less fit offspring; con- fects of stabilizing and disruptive selection? Here we ad- versely, stabilizing selection will favor negative assortment dress these questions using a meta-analysis of the strength (Dieckmann and Doebeli 1999; Kirkpatrick and Ravigne´ of assortative mating across diverse taxa of animals based 2002; Gavrilets 2004; De Cara et al. 2008; Otto et al. 2008). on a variety of assortment traits. For similar reasons, assortative mating can evolve in re- sponse to inbreeding or outbreeding depression (Epinat Methods and Lenormand 2009). Regardless of the type of selection involved, assortment can result from mutual mate choice We conducted a mixed-model meta-analysis of assortative or by the behavior of only males or females (McNamara mating based on phenotypic traits within natural animal and Collins
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