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