Download A theory of mate choice based on heterozygosity

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. Sarjeant, and two anonymous reviewers. I thank Jeff Nfitton for letting
me tee an unpublished chapter from his forthcoming book and the
National Science Foundation for its support.
REFERENCES
ADendorf FW, Leary RF, 1986. Heterozygosity and ftmen in natural
populationi of animals In: Conservation biology: the science of
scarcity and diversity (Soule ME, ed). Sunderland, Massachusetts:
Sinauer, 57-76.
Andersson M, 1982. Sexual selection, natural selection and quality
advertisement. BiolJ linn Soc 17375-393.
Andenson M, 1986. Evolution of condition-dependent sex ornaments
and mating preferences: sexual (election based on viability differences. Evolution 40-.804-816.
Anderston M, 1994. Sexual Selection. Princeton, New Jersey: Princeton University Press.
Avise J C 1994. Molecular marker*, natural history and evolution. New
York: Chapman & Hall.
Barnard CJ, FitzsimonsJ, 1989. Kin recognition and mate choice in
mice: fitnen consequences oJ mating with kin. Anim Behav 38:3540.
Bensch S, HauelquiH D, von Schantz T, 1994. Genetic similarity between parena predicts hatching failure: nonincestuous inbreeding
in the great reed warbler. Evolution 48:317-526.
Birkhead TR, Metier AP, 1992. Sperm competition in birds. Evolutionary causes and consequences. London: Academic Press.
Borgia C, 1979. Sexual selection and the evolution of mating systems.
In: Sexual selection and reproductive competition in social insects
(Blum MS, Blum NA, eds). New York: Academic Press; 19-80.
Brack O, Koref-Santibanez S, 1964. Miring activity of homo- and heterokaryotypes in DrasophUa pavani Genetics 49385-591.
Brooker MC, Rowley L Adams M, Baverstock PR, 1990. Promiscuity:
an inbreeding avoidance mechanism in a socially monogamous species. Behav Ecol SociobkJ 26:191-199.
Brown JL, 1983a. Cooperation—a biologist's dilemma. In: Advances
in the-study of behavior (Rosenblatt JS, Hinde RA, Beer C, Busnel
M, eds). New York: Academic Press; 1-37.
Brown JL, 1983b. Some paradoxical goals of cells and .organisms: the
role of the MHC In: Ethical questions in brain and behavior (Pfaff
DW, ed). New York: Springer-Verlag; 111-124.
63
Brown JL, Eklund A, 1994. Kin recognition and the major hiaocomparibiHty complex: an integrative review. Am Nat 143:170-196.
Charloworth B, 1988. The evolution of mate choice in a fluctuating
environment. J Theor Biol 130:191-204.
Charlesworth B, 1993. Inbreeding versus outbreeding. Evolution 47:
1896-1898.
Clarke GM, Brand GW, Whitten MJ, 1986. Fluctuating asymmetry: a
technique for measuring developmental stress caused by inbreeding. Aust J Biol Set 39:145-153.
Coopersmim CB, Lenington S, 1990. Preferences of female mice for
males whoje t-haplotype differs from their own. Anim Behav 40:
1179-1181.
Crocker G, Day T, 1987. An advantage to mate choke in the seaweed
fly, Codopa frigida. Behav Ecol Sociobtol 20:295-302.
Day TH, Budin RK, 1987. Non-random mating in natural populations
of the seaweed fty, Codopa frigida. Heredity 58:213-220.
Day TH, Mile. S, Pilkington MD, Budin RK, 1987. Differential mating
success in populations of seaweed flies (Codopa frigida). Heredity
58503-212.
Dobzhansky T, 1947. Genetics of natural populations. XIV. A response
of certain gene arrangements in the diird chromosome of D. psexkdootacum to natural selection. Genetics 42:142-160.
Dobzhansky T, Parlovsky O, Spassky B, Spassky N, 1955. Genedci of
natural populations XXUL Biological role of deleterious receaives
in populations of D. pstudoobscuru. Genetics 40:781-796.
Doherty PC, Zinkernagel RM, 1975a. A biological role for the major
histocompatibQity antigens. Lancet 1:1406.
Doherty PC, Zinkernagel RM, 1975b. Enhanced immunological surveulance in mice heterozygous at die H-2 gene complex. Nature
25630-52.
Ehrman L, Parsons PA, 1976. The genetics of behavior. Sunderiand,
Massachusetts: Sinauer Associates.
Ehrman L, Spiess EB, 1969. Rare type mating advantage in Dnuophila.
Am Nat 101:415-424.
Eklund AC, 1996. The effects of inbreeding on aggression in wild
male house mice (Mut domaticui). Behaviour 133:883-901.
Emlen JM, 1973. Ecology: an evolutionary approach. Reading, Massachusetts: Addison-Wesley.
Farr JA, 1980. Social behaviour patterns as determinants of reproductive success in the guppy, Potdha rtticulala (Pisces Poeciliidae).
Behaviour 7438-91.
Fkken RW, Fkken MS, Hailman JP, 1978. Differential aggression in
genetically different morphs of die white-throated sparrow (Zonotridda atticoUu). Zeit Tier 46:43-57.
Fisher RA, 1915. The evolution of sexual preference. Eugenics Rer 7:
184-192.
Fisher RA, 1930. The genetical theory of natural selection. Oxford:
Clarendon Press.
Folstad L Kaner AK, 1992. Parasites, bright males and the immunocompetence handicap. Am Nat 139:603-622.
Gilburn AA, Day TH, 1994. Evolution of female choice in seaweed
flies: Fisherian and good genes mechanisms operate in different
populations. Proc R Soc Lend B 255:159-165.
Hamilton WD, 1980. Sex versus non-tex versus parasite. Oikos 35:282290.
Hamilton WD, Zuk M, 1982. Heritable true fitness and bright birds:
a role for parasites? Science 218:384-387.
Haring V, Gray JE, McOure BA, Anderson MA, Clarke AE, 1990. Sdfincomparibuity: a self-recognition system in plants. Science 250:
937-941.
Harvey IF, Walsh KJ, 1993. Fluctuating asymmetry and lifetime mating
success are correlated in males of die damselfly Cotnagrion pudla
(Odonata: Coenagrionidae). Ecol Entomol 18:198-202.
Hill AVS, AUsopp EM, Kwiatkowski D, Anstey NM, Twumasi P, Rowe
PA, Bennett S, Brewster D. McMichael AJ, Greenwood BM, 1991.
Common West African HLA antigens are associated with protection
from severe malaria. Nature 352395-600.
Houtman AM, Falls JB, 1994. Negative assortative mating in the whitethroated sparrow: the effect of mate choice and inoasexual competition. Anim Behav 48377-383.
JaenikeJ, 1978. An hypothejij to account for die maintenance of sex within populations. Evol Theory 3:191-194.
Jimenez JA, Hughes KA, Alaks G, Graham L, Lacy RC, 1994. An experimental study of inbreeding depression in a natural habitat. Science 266:271-273.
64
Johnstone R, 1995. Sexual selection, honest advertisement and the
handicap principle: reviewing the evidence. Biol Rer 70:1-65.
Keane B, 1990. The efiect of rehurdnctt on reproductive success and
mate choice in the white-footed mouse, Puvmytau Itucopus. Anim
Behav 39:264-273.
Keller L, 1994. Rewards of promiscuity. Nature 372:229-230.
Keller LF, Arcese P, Smith JNM, Hochachka WM, Steama SC, 1994.
Selection against inbred song sparrows during a natural population
bottleneck. Nature 372356-357.
Kirkpatrick M, 1982. Sexual selection and the evolution of female
choice. Evolution 56:1-12.
Knapton RW, Falls JB, 1983. Difference! in parental contribution
among pair types in the polymorphic white-throated sparrow. Can
J Zool 61:1288-1292.
Knapton RW, Cartar RV, FaQs JB, 1984. A comparison of breeding
ecology and reproductive smrrts between morphs of the whitethroated sparrow. Wilson Bull 96^60-71.
Kopachena JC, Falls JB, 1993. Re-evaluation of morpb-apednc variations in parental behavior of the white-throated sparrow. Wilson
Bull 105:48-59.
Lande R, 1981. Models of speciation by sexual selection on polygenlc
traits. Proc Nad Acad Sd USA 783721-3725.
Lank DB, Smith CM, 1992. Females prefer larger lekc field experiments with ruffs (Phiiewiadau pugnax). Behav Ecol Sodobiol 30:
323-329.
Lank DB, Smith CM, Hanotte O, Burke T, Cooke F, 1995. Genetic
polymorphism for alternative mating behaviour in lekking male
ruff Ptahwuvhut pugnax. Nature 37839-62.
Leary RF, Allendorf FW, Knudsen KL, 1985. Inheritance of merutic
variation and die evolution of developmental stability in rainbow
trout. Evolution 39308-314.
Lenington S, 1991. The t complex: a story of genes, behavior, and
populations. Adv Study Behav 2031-86.
Lenington S, Coopenmith CB, Erhart M, 1994. Female preference
and variability among t-haptotypes in wild house mice. Am Nat 144:
766-784.
LowtherJK, 1961. Polymorphism in die white-throated sparrow, ZonotricMa aOicoBxs (Cmelin). Can J Zool 39:281-292.
Madsen T, Shine R, Loman J, Hakansson T, 1992. Why do female
adders copulate so frequently? Nature 355:440-441.
Manning JT, Hartley MA, 1991. Symmetry and ornamentation are correlated in the peacock's train. Anim Behav 42:1020-1021.
May RM, 1995. The cheetah controversy. Nature 374309-310.
Mitton JB, 1993a. Enzyme heterozygosity, metabolism, and developmental stability. Genetica 89:47-65.
Mitton JB, 1993b. Theory and data pertinent to the relationship between heterozygosity and fitness. In: The natural history of inbreeding and outbreeding (Thomhill NW, ed). Chicago: University of
Chicago Press; 17-41.
Mitton JB, 1994. Molecular approaches to population biology. Annu
Rev Ecol System 25:45-69.
Mitton JB, 1997. Selection in natural populations. Oxford: Oxford
University Press.
Mitton JB, Schuster WSF, Cothran EG, DeFriesJC, 1993. Correlation
between the individual heferozygosity of parents and their offspring. Heredity 7139-63.
Mailer AP, 1990. Fluctuating asymmetry in male sexual ornaments
may reliably reveal male quality. Anim Behav 40:1185-1187.
Meller AP, 1992. Female swallow preference for symmetrical male sexual onraments. Nature 357:238-240.
Meller AP, 1994a. Sexual selection and the barn swallow. New >brk:
Oxford University Press.
M0ller AP, 1994b. Sexual selection in die bam swallow (Hirundo rustiea). TV. Patterns of fluctuating asymmetry and selection against
asymmetry. Evolution 48:658-670.
Meller AP, Hogiund J, 1991. Patterns of fluctuating asymmetry in avian feather ornaments: implications for models of sexual selection.
Proc R Soc Lond B 245:1-5.
Mulvey M, Keller GP. Meffe GK, 1994. Single- and multiple-locus genotypes and fife-history responses of Gawtbusia holbndd reared at
two temperatures. Evolution 48:1810-1819.
O'Brien SJ, 1994. The cheetah's conservation controversy. Conserv
Biol 8:1153-1155.
O'Donald P, 1962. The theory of sexual selection. Heredity 17341552.
Behavioral Ecology Vol. 8 No. 1
O'Donald P, 1967. A general model of sexual and natural selection.
Heredity 22:499-518.
Olsson M, Madsen T, Shine R, Gullberg A, Tegelstrdm H, 1994. Can
female adders multiply? Nature 369328.
Partridge L, 1983. Non-random mating and offspring fitness. In: Mate
choice (Bateson P, ed). Cambridge: Cambridge University Press;
227-255.
Petrie M, 1994. Improved growth and survival of offspring of peacocks
with more elaborate trains. Nature 371398-599.
Pomiankowski A, 1990. How to find the top male. Nature 547:616617.
Pomiankowski A, Meller AP, 1995. A resolution of the lek paradox.
Proc R Soc Lond B 260-51-29.
Potts WK, Manning q , Wakeland EK, 199.1a. The evolution of MHCbased mating preferences in Mus. In: Molecular evolution of die
major hUtocompatibiliry complex (Klein J, Klein D, eds). Berlin:
Springer-Verlag; 421-434.
Potts WK, Manning CJ, Wakeland EK, 1991b. Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature
35fc619-621.
Potts WK, Wakeland EK, 1993. Evolutkm of MHC genedc diversity: a
tale of incest, pestilence and sexual preference. Trends Genet 9:
408-412.
Rails K, BaDou JD, Templeton A, 1988. r«rimati^ of die cost of inbreeding in mammals Conserv Biol 2:185-193.
Schaal BA, Levin DA, 1977. Population structure and local differentiation in Liatris cj&ndmcta. Am Nat 110:191-206.
Schulze-Hagen K, Swatschek I, Dyrcz A. Wink M, 1993. Multiple Vaterschaften in Bruten des Seggenrohrsangers Acwaphahu pahidicotaji Omithol 1^4:145-154.
Scribner KT, Smith MH, 1990. Genetic variability and antler development. In: Horns, pronghornj, and anders (Bubenik GA, Bubenik
AB, eds). New tort Springer-Verlag; 460-473.
ScribneT KT, Smith MH, Johns PE, 1989. Environmental and genedc
components of antler growth in white-tailed deer. J Mammal 70:
284-291.
SerradillaJM, Ayala FJ, 1983. Alloprocopdc selection: a mode of natural selection promoting polymorphism. Proc Nad Acad Sd USA
80:2022-2025.
Shields WM, 1993. The natural and unnatural history of inbreeding
and outbreeding. In: The natural history of inbreeding and outbreeding (Thomhill NW, ed). Chicago: University of Chicago Press;
143-169.
Shutter SM, Wade MJ, 1991. Equal mating success among male reproductive strategies in a marine isopod. Nature 350:608-610.
Smith DAS, 1975. Sexual selection in a wild population of die butterfly Danmu dajappus L. Sdence 187:664-665.
Smith DAS, 1981. Heterozygous advantage expressed through sexual
• selection in a polymorphic African butterfly. Nature 289:174-175.
Spiess E, Linger B, 1966. Mating control by gene arrangements in
Drosophila pstudooiaam. Genetics 54:1139-1149.
Templeton AR, 1986. Coadaptadon and ombreeding depression. In:
Conservation biology: die sdence of scarcity and diversity (Soule
ME, ed). Sunderland, Massachusetts: Sinauer Associates; 105-111.
Thorneyeroft HB, 1966. Chromosomal polymorphism in die whitethroated sparrow, ZonotruJaa aWicoiiU. Sdence 154:1571-1572.
Thorneycroft HB, 1975. A cytogenetic study of die white-throated
sparrow, ZonotriMa albicollis (GmeHn). Evolution 29:611-621.
Thomhill NW (ed), 1993. The natural history of inbreeding and outbreeding. Chicago: University of Chicago Press.
Trivers RL, 1972. Parental investment and sexual selection. In: Sexual
selection and die descent of man 1871-1971 (Campbell B, ed).
Chicago: Aldine; 136-179.
Watson PJ, 1991. Multiple paternity as genetic bet-hedging in female
sierra dome spiders, Lhityphia Htigiosa (linyphiidae). Anim Behav
41343-360.
Watt WB, Carter PA, Blower SM, 1985. Adaptation at specific lod. IV.
Differential mating success among gtycolytic allozyme genotypes of
CoBas butterflies. Genetics 109:157-175.
Watt WB, Carter PA, Donohue K, 1986. Females' choice of "good
genotypes" as mates is promoted by an insect mating system. Science 233:1187-1190.
Wedekind C, 1994. Handicaps not obligatory in sexual selection for
rrptranrr genes. J Theor Biol 17037-62.
Whillans KV, Falls JB, 1990. Effects of male removal on parental care
Brown • Mate choice and heterozygosity
of female white-throated sparrows Zonatridua albirolht Anim Behav
S9-.869-878.
Wilcockson RW, Crean CS, Day TH, 1995. Heritabflity of a sexually
selected character expiesaed in both sexes. Nature 374:158-159.
Wildt DE. Bush M, Goodrowe KL, Packer C Pusey AE, Brown JL,
Joslin P, O'Brien SJ, 1987. Reproductive and genetic consequences
of founding isolated lion populations. Nature 329:328-331.
Williams GC, 1966. Adaptation and natural selection. Princeton, New
Jersey: Princeton University Press.
YunazaH K, Boyse EA, Mike V, Thaler HT, Mathieson BJ, AbboaJ,
65
Boyse J, Zayas ZA, 1976. Control of mating preferences in mice by
genes in the major histocompadbility complex. J Exp Med 144:
1324-1335.
Zahavi A, 1975. Mate selection—a selection for a handicap. J Theor
Biol 53:205-214.
Zahavi A, 1977. The cost of honesty (further remarks on the hanHirap
principle). J Theor Biol 67:603-605.
Zuk M, 1994. Immunology and the evolution of behavior. In: Behavioral mechanisms in evolutionary ecology (Real LA, ed). Chicago:
University of Chicago; 354-368.