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Behavioral Ecology VoL 8 No. 1: 60-65 A theory of mate choice based on heterozygosity Jerram L. Brown Department of Biological Sciences, State University of New York, Albany, NY 12222, USA In theories of mate choice that rely on genetic benefits, the nature of the "good genes" involved has received little attention. A review of genetic studies of mate choice in a variety of species and situations suggests that individual heterozygosity is more important than previously realized. Females are predicted to value heterozygosity in their offspring and under some conditions in their males. The expression of vigor, condition-sensitive ornaments, and symmetry in males may be a direct reflection not of "good genes" but of individual heterozygosity at key loci or at many loci. Like sexuality itself, mate choice based on heterozygosity and genie diversity may be an adaptation that favors the production of diverse and superior competitors. Female choice is made meaningful by sexuality, and the adaptive value of choice probably depends on some of the same factors that maintain sexuality. Key words: genetic quality, heterozygosity, mate choice, sexual selection. [Bthav Ecol 8:60-65 (1997)] T he manner by which sexual selection acts on mate choice and the factors that influence choice are not yet clear (Andersson, 1994). Although other processes have been suggested, debate and empirical work have centered on the evolution of sexually dimorphic traits by mechanisms underlying the "good genes" process, such as condition-sensitive mating (Andersson, 1982, 1986; Emlen, 1973; Fisher, 1915, 1930; Johnstone, 1995; Williams, 1966; Zahavi, 1975, 1977), or on the runaway process (Fisher, 1915, 1930; Kirkpatrick, 1982; Lande, 1981; O'Donald, 1962, 1967). This paper focuses on the choosing sex, assumed for simplicity to be female, rather than on the chosen (male) sex and its ornaments. With these approaches, the implicit assumptions have usually been made that males can be ranked according to their standing in the population and that the task of the female is to find and mate with the highest ranking male possible under her circumstances (Pomiankowski, 1990), the one that will confer on her offspring the greatest vigor and health (good genes process) and the greatest attractiveness of sons to females (runaway process). These processes are thought to carry "good genes" (for vigor), ornament genes, and "preference genes" to fixation. I put aside the idea that there is a best male and that he is best for every female. Instead, I shall develop three related ideas: (1) What is best for one female may not be best for another; (2) even if the "best" male is found, his superiority may be due to heterozygosity at one or more loci, hence not simply heritable (heterozygosity is not an allele); (3) mate choice amplifies the chief advantage of sexuality, namely, genetic diversification. Following from these ideas, I argue that a female's strategy should be to find the alleles that best complement her own in at least some of her offspring. Often this means choosing a mate so that genes in her offspring will be heterozygous at some or many loci. This paper develops this latter perspective, which I call the "heterozygosity theory," documenting the plausibility of the processes with data from a variety of studies. The heterozygosity approach leads to consideration of mate choice in relation to theories for the maintenance of sex. One of the costs of sex is the genetic load of deleterious, recessive alleles. Choice of a mate so as to increase heterozygosity in the offspring can reduce the negative effects of those alleles. Furthermore, the chief benefit of sex according to theory is Received 10 August 1995; accepted 20 March 19%. 1045-2249/97/J5.00 C 1997 International Society for Behavioral Ecology genetic diversification of offspring so as to be better prepared for unpredictable interactions faced in the next generation (Hamilton, 1980; Jaenike, 1978). Mate choice in general magnifies this benefit by introducing new genetic material and allowing superior gametes from each sex to unite. Thus, when sex is important, mate choice should amplify its benefits. Should a female then prefer males who are more heterozygous? The answer is "not necessarily" in terms of number of mature offspring; Partridge (1983) formally proved that female choice based on male genotype would not affect the averagefitnessof the progeny at a single diallelic locus with heterozygous advantage, assuming that selection occurs before mating. More of these offspring would, however, be heterozygous at most allele frequencies (Borgia, 1979; Mitton et al., 1993), and there could still be an additional advantage in the competitiveness of the adult heterozygous offspring when mating, hi a fluctuating environment with a long-term measure of fitness, the fitness of progeny of heterozygous males is greater than the population mean fitness, and femalechoice alleles that favor heterozygous males are selected under most conditions (Charlesworth, 1988). A similar result occurs when selection depends on the relative production of the most-fit genotypes (Mitton, 1997). As with all genetic models of selection, the danger of exhausting genetic variation in the population exists. However, as long as many independently segregating, overdominant loci are present, the genetic system does not readily come to equilibrium and exhaust genetic variation, especially in a changing environment (Charlesworth, 1988; Mitton, 1993b; Pomiankowski and Mdller, 1995). It is therefore useful to examine empirical studies that treat heterozygosity in relation to male competitiveness and female choice. Some advantages of symmetry and heterozygosity Heterozygosity is generally beneficial to individuals across a wide range of species (reviewed by Avise, 1994; Mitton, 1993b, 1994). Developmental homeostasis measured as fluctuating asymmetry or measured by other methods increases with enzyme heterozygosity in most species that have been investigated (Mitton, 1993a). In a sample of 21 species of animals, superior survival of individuals was associated with heterozygosity in 17 species (AUendorf and Leary, 1986). Survival advantages were associated with superior disease resistance, growth rate, and developmental stability. In three salmonidfishesand a cyprinodontid fish, heterozygosity reduced fluctuating asym- Brown • Mate choice and hetcrorygosity metry (Leary et aL, 1985; Mulvey et aL, 1994). Experimental reduction of heterozygosity by inbreeding increased fluctuating asymmetry in a diploid copepod but not in a haplodiploid bee (Clarke et aL, 1986). One of the most convincing studies was done on the herb Liatris cjtindracrus, age at sexual maturity, reproductive output and vegetative output were all correlated with individual heterozygosity (Schaal and Levin, 1977). These lines of evidence suggest that the documented success in mating by more symmetrical or more ornamented males of many species (Andersson, 1994; Harvey and 'Walsh, 1993) has its genetic basis not so much in "better" genes as in greater heterozygosity. By promoting greater developmental stability and Hi*p««y resistance, heterozygosity may contribute in a major way to the superior condition of the more successful males. Heterozygosity appears to underlie the superiority of males with respect to developmental stability (judged by symmetry), disease resistance, general condition and attractiveness. By identifying heterozygosity as a key genetic factor of central importance a new perspective is created and new, testable questions arise. If these predictions are widely supported, we may conclude that male ornaments are indicators of genetic heterozygosity and that is why females attend to them. Active avoidance of homosygoshy by choice 61 tage simply because they are rare or novel. Examples have been suggested in Drosophila (Ehrman and Parsons, 1976; Ehrman and Spies*, 1969), although doubt exists about their relevance in nature (reviewed by Partridge, 1983). Male guppies (Pota&a nticulata) are known for their phenotypic diversity, and Farr (1980) has suggested that a female's preference for rare males might increase the heterozygosity of her offspring and their ability to tolerate a variable environment A mating system that maximizes heterozygosity among offspring is the mating between "opposite" or different homozygotes (Serradilla and Ayala, 1983). This pattern seems unlikely in general in nature (however, see Gilburn and Day, 1994), but it may be approximated in some ways. In some systems females act in a way that seems to reduce homozygosity at specific loci. Female house mice that are heterozygous for the lethal t complex tend to avoid producing offspring that are homozygous for the t complex by preferring not to mate with males that carry the same haplotype (Lenington, 1991). The preference for non-t males is weaker when the lethal effect is weaker (Coopersmith and Lenington, 1990; Lenington et aL, 1994). A gene for this specific choice has been mapped to the t complex (Lenington S, personal communication). White-throated sparrows (Zonotridaa albitoiUs) have two color morphs, white-striped and tan-striped, that are controlled by a chromosomal inversion (Thorneycroft, 1966, 1975). Homozygous white-striped individuals are extremely rare, suggesting that homozygous white might often be lethaL Tan-striped birds are homozygous recessive. Almost invariably, tan-striped sparrows mate with white-«triped sparrows; thus homo-karyotypic matings are rare (Houtman and Falls, 1994; Knapton et aL, 1984; Lowther, 1961). The mechanism by which matings between morphs of the same type are avoided is not yet clear, but it probably involves the fact that tan-striped morphs are better at parental care (Knapton and Falls, 1983; Kopachena and Falls, 1993; Whillans and Falls, 1990), and white-striped morphs are better in aggressive contexts (Ficken et al., 1978). Interestingly, the t haplotype male mouse is also superior in aggressive contexts, and this is also determined by a chromosomal inversion. Here is another example in which the best mate for an individual depends on its own genotype. White-striped individuals profit from being mated to a good parent (tan), and tan birds may profit from the greater aggressiveness of white-striped mates and offspring. There is much evidence for the heterozygosity theory that is concerned with avoidance of inbreeding. In a variety of species, females prefer males that are not too closely related (e.g., Ptwmyscus leucopxis, Keane, 1990; and the literature on optimal in- and outbreeding reviewed by Shields, 1993; Templeton,1986). Although the advantage to parents of avoiding inbreeding is greater offspring vigor, as in the good genes process, it is not achieved simply by choosing the most vigorous male. Vigor is achieved by avoiding homozygosity. A basic tenet of inbreeding avoidance is self-reference or family reference, where possible. They are achieved by a variety of mechanisms, including self-incompatibility systems in plants (Haring et aL, 1990) and various behavioral phenomena in animals. Recent research suggests that histocompatibility genes may play an important role in the avoidance of inbreeding in mamVnaU and tunicates (reviewed by Brown and Eklund, 1994), but many other behavioral mechanisms also hinder inbreeding (ThornhM, 1993). In the more conventional view, inbreeding avoidance mechPassive avoidance of homozygosity anisms are used to reduce the probability of homozygous genes with a lethal or deleterious effect. In a broader perThe fixation assumption of the good-genes process is not satspective, however, avoidance of close inbreeding may also proisfied when females actively avoid males who carry alleles that duce offspring that are better competitors by virtue of general are likely to be similar to their own. Active avoidance is not, heterozygosity at loci shared by kin in wild deer mice (Ptrohowever, the only mechanism by which "good genes" are premyscus spp.; Jimenez et aL, 1994), house mice (Mui muscuhu; vented from going to fixation. When macho-male strategies Barnard and Fitzsimons, 1989; Eklund, 1996), and birds (Kelbecome extreme, alternative strategies may be favored by freler et aL, 1994). quency-dependent selection (Uopod: Paracercas seutpta, Shuster and Wade, 1991; ruff: Philomackus pugnax. Lank and In a behavioral context, inbreeding is usually conceived acSmith, 1992; Lank et aL, 1995). Again, the genes for the "best cording to pedigree relationships. But inbreeding has a dif-males" do not go to fixation, and genetic diversity is mainferent meaning to population geneticists, who are more contained. If such systems are really at equilibrium, then females cerned with deviations from random mating (Chariesworth, gain no advantage from mating with the morph that seems to 1993). Even in this latter context, inbreeding can be deletebe in the best condition; sneaky tactics might have equal fitrious. Reed warblers (Acrocephatus sdrpaaus) with a high deness. gree of band-sharing in ONA fingerprints (and no known pedigree connections) suffered a lower hatching rate (Bensch et Another mechanism that prevents fixation of good genes is aL, 1994), and populations that have passed through an exheterozygote advantage in mating contests. When this applies tended bottleneck are sometimes thought to have reduced to phenotypes of mating males, the best male may be heterofertility (May, 1995; O'Brien, 1994; Rails et aL, 1988; Wildt et zygous, making it impossible for good genes to reach fixation, al., 1987) as for example, in sulfur butterflies (CoHas spp.; Wan et aL, 1985, 1986 as analyzed by Mitton, 1993b). Males that were In another model for frequency-dependent mating success, heterozygous at the pgi locus for certain alleles were generally some phenotypes have been hypothesized to have an advan- Behavioral Ecology Vol. 8 No. 1 62 better flyers and achieved a greater proportion of matings than expected by random mating. Although there may be a best genotype in such a system, there is no best allele; and genetic variability at this locus is maintained by heterosis. Heterosis in mating contests may maintain other chromosomal polymorphisms that have behavioral effects, such as the mating types of seaweed flies (Codopa frigida, Crocker and Day, 1987; Day and Butlin, 1987; Day et aL, 1987; Wilcockson et al., 1995). Similarly, in the African butterfly, Danaus ckrysippus, a heterozygous color-pattern gene was associated with a mating advantage in males (Smith, 1975,1981). Again, good genes do not go to fixation, and goodness depends on heterozygosity. In Drosophtia, early work revealed that flies heterozygous for certain common inversions (heterokaryotypes) bad higher fitness than homokaryotypes (Dobzhansky, 1947). Dobzhansky et al. (1955) proposed a general advantage of heterozygosity due to masking of sublethals. These advantages could be traced in large part to mating behavior (Ehrman and Parsons, 1976). In D. pavani, the frequency of heterokaryotypes was significantly higher among males that courted or mated than among those who did not (Brncic and Roref-Santibanez, 1964). Heterokaryotypic males of D. pstudoobscwra mated more rapidly (Spiess and Langer, 1966). Promotion of heterozygosity by multiple When self-reference is not possible and novel male phenotypes are not discernible, a female can increase her chances of having some heterozygous offspring by mating with a variety of males, a mechanism that has been proposed for snakes (Madsen et al., 1992) and lizards. In lizards, offspring of females who were promiscuous had a higher hatching rate, higher survival, and a lower frequency of malformations (Olsson et al., 1994; Keller, 1994). Although much attention has been given to mixed-male strategies (Trivers, 1972), little attention has been given to mixed-female strategies. It seems reasonable that a female's first priority is resources or a territory in which to breed; but once she has that, she may seek to improve the genetic quality of some of her offspring by diversifying the genes of males chosen as parents for her offspring. Thus, she may mate with the owner of the territory and with other nearby males as in house mice (Potts et aL, 1991a,b), splendid fairy wren* (Maiurus splendent, Brooker et al., 1990), aquatic warblers (Aeroctphalus pahidicola, Schulze-Hagen et aL, 1993) and many other birds (Birkhead and Mailer, 1992). When resources are not at stake, females may mate with one male first to ensure fertilization and with subsequent males to improve offspring quality (Watson, 1991). The result in all these cases will be genetic diversification of the brood. Immunology, beteroxygosity, and offspring quaHty The immune system has been implicated in mate choice in two ways. First, because the major histocompatibih'ty complex (MHC) has been implicated in disassortative mate choice framazaki et aL, 1976) it was hypothesized to be the basis of a mechanism for kin recognition used to avoid inbreeding (Brown, 1983a,b). Second, because bright plumage in birds was thought to indicate good health resulting from resistance to parasites, bnght-plwaagad birds were hypothesized to have superior disease resistance (Hamilton and Zuk, 1982) and better immune systems (Folstad and Karter, 1992). These theories each stimulated further research (Brown and Eklund, 1994; Zuk, 1994), but the significance of a connection between them has been little appreciated. I show here that the two hypotheses are closely related and discuss some evolutionary implications of this connection. Both the MHC hypothesis and the parasite-resistance hypothesis are based on the assumption that a female should prefer to mate with males whose genes confer greater vigor, health, and competitive ability on her offspring. The inbreeding and parasite hypotheses overlap in some ways, but they differ in the mechanisms invoked. Under the inbreeding hypothesis, an animal prefers a mate that differs from itself in MHC haplotype, without regard to signal strength, signal cost, or handicap (Wedekind, 1994), thus raising heterozygosity among the offspring and in the population. The advantages of MHC-based choice are twofold: enhanced disease resistance (Doherty and Zinkernagel, 1975b; Hill et aL, 1991) and reduced manifestation of deleterious alleles, thus producing offspring that are more competitive (Potts and Wakeland, 1993). Under the parasite hypothesis, the emphasis is on signal strength and cost While direct effects on the MHC were not specified, they are implicit because of the known relationship between the MHC and resistance to parasites and disease. Evidence u accumulating that both inbreeding avoidance and female choice on the basis of "bright coloring" produce offspring that are more competitive. Outbred offspring of mice are superior competitors in nature (Jimenez et aL, 1994), as well as in the lab (Barnard and Fitzsimons, 1989; Eklund, 1996). In birds, young fathered by males with the brightest plumage and greater symmetry survive better (Manning and Hartley, 1991; Petrie, 1994). In choice versus nochoice experiments, choice generally yields higher offspring fitness, although results can be clouded by doubt about which kind of sexual selection is operating (reviewed by Andersson, 1994). Generalization and prediction Several lines of evidence described above suggest that females in sexually monomorphic as well as in dimorphic species tend to prefer mates whose genetic contributions are likely to diversify the genotypes of the progeny by promoting heterozygosity. In choosing genetically dissimilar mates, females promote offspring heterozygosity at many loci in their offspring. As heterozygosity increases, the number of different genes, or genie diversity, brought to the progeny is also likely to increase. Heterozygosity may benefit individuals by masking lethal and sublethal genes, while genie diversity may benefit them by providing a wider range of potentially useful gene products, as has been suggested for the MHC (Doherty and ZinkernageL 1975a). These twin goals of homozygosity avoidance, namely, heterozygosity and genie diversity, are consistent with current thinking about the role of sex in promoting genetic diversity in an ever-changing environment (Hamilton, 1980;Jaenike, 1978). Sexual dimorphism is not conspicuous in those species that minimize homozygosity either by avoidance of inbreeding or by avoidance of learned familial genetic markers (e.g., t complex, MHC). Species in which sexual selection for male traits appears to be extreme may utilize different ways to achieve heterozygojity and genie diversity in their offspring. In many of these species, situations may not permit choice based on genetic markers or learned familial associations, but females can still take advantage of the same relationship between homozygosity and competitiveness by turning it around In choosing or accepting the most competitive males, females are likely to be getfing males of above-average heterezygesity. For . example, in white-tailed deer (Odocoileus xrirgmianus) body size and development of antlers are greatest in the most heterozygous males (Scribner and Smith, 1990; Scribner et al., 1989). This deduction is supported by the experimentally ver- Brown • Mate choice and heterozygosity ified relationship between heterozygosity and competitiveness, and it is consistent with the recently demonstrated positive relationship between bilateral symmetry in sexually selected male traits and female preference for those traits (for example, in the barn swallow, Hirundo rustxca, Meller, 1990, 1992, 1994a,b; Meller and Hoglund, 1991; and possibly in a damselfly; Harvey and Walsh, 199S). The heterozygosity theory attempts to identify the essence of genetic quality. It leads to the following general prediction: Traits of all kinds that are used by females when Judging males reach their extreme expression in males with the greatest average heterozygosity. More specifically, I predict that if the heterozygosity theory is correct, male ornament expression, symmetry of ornaments, and male mating success in a large population will positively correlate with degree of individual heterozygosity. The heterozygosity theory allies mate choice more clearly with the dominant theory of sexuality than do previous theories. It helps unify die study of mate choice by extending it to situation* in which sexual dimorphism is not die issue, as in avoidance of inbreeding. Regardless of the role that heterozygosity may play in mate choice and sexual selection, it is time thai empiricists began investigating genetically based hypotheses to explain die relationship of mate choice to genetic quality. For useful dlminton and comment! on the manuscript, I thank Esther Brown, Nirmal Bhagabati, Lee Dugatkm, Shou-hslen LLJeffMltton, Kevin Omland, memben of the SUNY-Albany Animal Social Systems course, J. Alexander, PJC Kaianth, M. Reff, T. Sanders, M. 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