Mate Choice and Genetic Quality: A Review of the Heterozygosity Theory

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This chapter presents a review of mate choice and genetic quality, defines mate choice, and discusses some of the key issues about how individuals can benefit from being choosy, including the distinction between two main types of genetic benefits. It also focuses on heterozygosity and fitness and presents an overview of the methods that have been used to estimate individual heterozygosity or relatedness among individuals. It also presents a review of the studies that have found correlations between individual heterozygosity and a variety of fitness‐related traits. The chapter consists of two parts—mate choice based on relatedness with the partner, which is choice to optimize offspring heterozygosity and the link between the evolution of promiscuity and inbreeding avoidance.

Introduction

Mate choice has been and still is a very popular research topic in behavioral and evolutionary ecology. This is not surprising, given the role it plays in our own lives, and given its importance for understanding phenomena ranging from sperm form and function (Holman and Snook, 2006) to speciation (McPeek and Gavrilets, 2006). Research on mate choice beautifully illustrates how theoretical work in the form of verbal and mathematical models develops alongside simple and more sophisticated empirical studies (e.g., Gustafsson 2006, Kokko 2006, Qvarnström 2006). The study of mate choice has also created its share of scientific debate and controversy, as can be seen in the literature, and observed at scientific conferences. As a graduate student, I witnessed (from a safe distance) some surprisingly emotional exchanges about why females paired with an already mated male, and later I myself got caught up in discussions about whether and how females benefit from engaging in extra‐pair copulations. A lively research field it is indeed.

Arguably the most controversial issue of all is the importance of indirect genetic benefits for the evolution of mate choice. The key questions are these. Are genetic benefits important enough to explain the evolution of more or less sophisticated (and costly) choice mechanisms? What is the nature of these genetic benefits? The main aim of this review is to consider a specific type of genetic benefit, namely the fitness gains resulting from the production of offspring with higher individual genetic diversity (heterozygosity). Research on inbreeding and on the relationship between individual heterozygosity and fitness‐related traits in free‐living populations has blossomed, particularly after molecular tools such as microsatellite markers became widely available. However, we are only beginning to understand why individual heterozygosity is related to fitness and how this affects the evolution of mate choice.

To set the stage for this review, I briefly define mate choice, and discuss some of the key issues about how individuals can benefit from being choosy, including the distinction between two main types of genetic benefits (Section II). The next section focuses on heterozygosity and fitness. Here, you will find an overview of the methods that have been used to estimate individual heterozygosity or relatedness between individuals, and a summary of an ongoing debate about the importance and interpretation of heterozygosity–fitness correlations. Section III also contains a review of studies that have found correlations between individual heterozygosity and a variety of fitness‐related traits. Section IV is about mate choice and heterozygosity and consists of two parts. In the first part, I discuss mate choice based on relatedness with the partner, that is, choice to optimize offspring heterozygosity. I consider when it will pay females to mate with a more or less‐related male, and how females should trade off choice for different types of genetic benefits. Then, I emphasize the link between the evolution of promiscuity and inbreeding avoidance, and I discuss why it is important to consider the costs and mechanisms of choice. Finally, I review the evidence that social mate choice, choice of a copulation partner, and choice of sperm under multiple mating depends on relatedness. The second part of Section IV is about mate choice favoring heterozygous partners. First, I discuss why one should expect such choice and why the heterozygosity of the choosing female may affect her choice. Then, I review the evidence that individuals prefer heterozygous mates, in different contexts.

This review is probably biased toward studies on birds, because those are the studies I am most familiar with. However, I attempted to review the entire recent literature, and the fact that many examples are from birds also reflects the relative amount of research on avian mate choice.

Section snippets

What is Mate Choice?

There is still considerable debate about the existence and relative importance of the different mechanisms of choice, and particularly about how to define and demonstrate “cryptic choice” (e.g., Birkhead 1998, Birkhead 2000, Birkhead 2002, Bussière 2006, Kempenaers 2000, Pilastro 2004, Pitnick 2000, Telford 1998). However, in general, three types of choice can be distinguished.

  • 1

    Choice of a social partner or a copulation partner (precopulatory, prefertilization). This is what we commonly

Heterozygosity and Fitness

The heterozygosity theory suggests that individuals benefit from choosing a mate that will maximize heterozygosity at some or many loci in the offspring (Brown, 1997). Such benefit would arise if a positive correlation between individual heterozygosity and fitness exists. A special case of heterozygote advantage is referred to as hybrid vigor or heterosis. This stems from the observation that offspring from crosses between two breeding lines (e.g., in agriculture or animal breeding) often show

Theoretical Considerations

If individual heterozygosity generally correlates with fitness under circumstances that are often found in natural populations, females (and males) would clearly benefit from maximizing (or optimizing) the heterozygosity of their offspring. Many empirical studies have attempted to test this, and I review them below after first discussing some other issues that have an impact on the evolution of mate choice for heterozygosity.

Conclusions and Outlook

In this review, I addressed the hypothesis that mate choice is linked to genetic compatibility. Synthesizing the evidence reviewed above, it is clear that mate choice processes can lead to increased offspring heterozygosity, and that this can be beneficial. However, the current data are still insufficient to make sweeping statements about the generality of the heterozygosity hypothesis. It is noteworthy that many studies have tested multiple predictions, but found evidence for only one (if at

Acknowledgments

I sincerely thank Axel Krikelis and Renate Alton for library assistance, Heike Gorny‐Leimpeters and Anke Hundrisser for secretarial assistance, Theo Weber for redrawing the figures, and the members of my group, particularly James Dale, Emily DuVal, Wolfgang Forstmeier, Jakob Mueller, and Mihai Valcu for stimulating discussions over breakfast, coffee, lunch, tea and dinner, and for insightful comments on an earlier version of the manuscript. I am grateful to Tom Van de Casteele, who kindly

References (321)

  • C. Edly‐Wright et al.

    Genetic similarity of mates, offspring health and extrapair fertilization in house sparrows

    Anim. Behav.

    (2007)
  • M.J.G. Gage et al.

    Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus

    Curr. Biol.

    (2006)
  • J. Goudet et al.

    The correlation between inbreeding and fitness: Does allele size matter?

    Trends Ecol. Evol.

    (2002)
  • K. Acevedo‐Whitehouse et al.

    Disease susceptibility in California sea lions

    Nature

    (2003)
  • P.B. Aeschlimann et al.

    Female sticklebacks Gasterosteus aculeatus use self‐reference to optimize MHC allele number during mate selection

    Behav. Ecol. Sociobiol.

    (2003)
  • W. Amos et al.

    The influence of parental relatedness on reproductive success

    Proc. Roy. Soc. Lond. B

    (2001)
  • M. Andersson

    “Sexual Selection.”

    (1994)
  • V. Apanius et al.

    The nature of selection on the major histocompatibility complex

    Crit. Rev. Immunol.

    (1997)
  • J.M. Aparicio et al.

    What should we weigh to estimate heterozygosity, alleles or loci?

    Mol. Ecol.

    (2006)
  • K.D. Arkush et al.

    Resistance to three pathogens in the endangered winter‐run Chinook salmon (Oncorhynchus tshawytscha): Effects of inbreeding and major histocompatibility complex genotypes

    Can. J. Fish. Aquat. Sci.

    (2002)
  • P. Armbruster et al.

    Inbreeding depression in benign and stressful environments

    Heredity

    (2005)
  • P. Armbruster et al.

    Equivalent inbreeding depression under laboratory and field conditions in a tree‐hole‐breeding mosquito

    Proc. Roy. Soc. Lond. B

    (2000)
  • G. Arnqvist et al.

    The evolution of infidelity in socially monogamous passerines: The strength of direct and indirect selection on extrapair copulation behavior in females

    Am. Nat.

    (2005)
  • J. Aspi

    Inbreeding and outbreeding depression in male courtship song characters in Drosophila montana

    Heredity

    (2000)
  • M.C. Audo et al.

    Effect of quantity of enviromental‐stress on multilocus heterozygosity growth relationships in Eisenia‐Fetida (Annelida, Oligochaeta)

    Heredity

    (1995)
  • L. Avilés et al.

    Group living and inbreeding depression in a subsocial spider

    Proc. Roy. Soc. Lond. B

    (2006)
  • F. Balloux et al.

    Does heterozygosity estimate inbreeding in real populations?

    Mol. Ecol.

    (2004)
  • C.A. Barber et al.

    A test of the genetic compatibility hypothesis with tree swallows, Tachycineta bicolor

    Can. J. Zool.

    (2005)
  • P. Bateson

    Preferences for cousins in Japanese quail

    Nature

    (1982)
  • P. Bateson

    Optimal outbreeding

  • K. Bean et al.

    Patterns of parental relatedness and pup survival in the grey seal (Halichoerus grypus)

    Mol. Ecol.

    (2004)
  • S. Bensch et al.

    Genetic similarity between parents predicts hatching failure: Nonincestuous inbreeding in the great reed warbler?

    Evolution

    (1994)
  • G. Bernasconi et al.

    Evolutionary ecology of the prezygotic stage

    Science

    (2004)
  • N. Bierne et al.

    An inbreeding model of associative overdominance during a population bottleneck

    Genetics

    (2000)
  • T.R. Birkhead

    Cryptic female choice: Criteria for establishing female sperm choice

    Evolution

    (1998)
  • T.R. Birkhead

    Defining and demonstrating postcopulatory female choice—again

    Evolution

    (2000)
  • T.R. Birkhead et al.

    Postcopulatory sexual selection

    Nat. Rev. Genet.

    (2002)
  • T.R. Birkhead et al.

    Nontransitivity of paternity in a bird

    Evolution

    (2004)
  • J.D.D. Bishop et al.

    Female control of paternity in the internally fertilizing compound ascidian Diplosoma listerianum. II. Infestigation of male mating success using RAPD markers

    Proc. Roy. Soc. Lond. B

    (1996)
  • J.M. Bishop et al.

    Social common mole‐rats enhance outbreeding via extra‐pair mating

    Biol. Lett.

    (2007)
  • J. Blais et al.

    Nonlinear effects of female mate choice in wild threespine sticklebacks

    Evolution

    (2004)
  • D. Blomqvist et al.

    Genetic similarity between mates and extra‐pair parentage in three species of shorebirds

    Nature

    (2002)
  • C. Bonneaud et al.

    Complex Mhc‐based mate choice in a wild passerine

    Proc. Roy. Soc. Lond. B

    (2006)
  • C. Bonneaud et al.

    Major histocompatibility alleles associated with local resistance to malaria in a passerine

    Evolution

    (2006)
  • A. Bretman et al.

    Molecular evidence of post‐copulatory inbreeding avoidance in the field cricket Gryllus bimaculatus

    Proc. Roy. Soc. Lond. B

    (2004)
  • J.V. Briskie

    Spatiotemporal patterns of sperm storage and last‐male sperm precedence in birds

    Funct. Ecol.

    (1996)
  • H.B. Britten

    Meta‐analyses of the association between multilocus heterozygosity and fitness

    Evolution

    (1996)
  • M.G. Brooker et al.

    Promiscuity: An inbreeding avoidance mechanism in a socially monogamous species?

    Behav. Ecol. Sociobiol.

    (1990)
  • J.L. Brown

    A theory of mate choice based on heterozygosity

    Behav. Ecol.

    (1997)
  • J.L. Brown

    The new heterozygosity theory of mate choice and the MHC

    Genetica

    (1999)
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