The aim of this review is to consider the potential benefits that females may gain from mating more than once in a single reproductive cycle. The relationship between non-genetic and genetic benefits is briefly explored. We suggest that multiple mating for purely non-genetic benefits is unlikely as it invariably leads to the possibility of genetic benefits as well. We begin by briefly reviewing the main models for genetic benefits to mate choice, and the supporting evidence that choice can increase offspring performance and the sexual attractiveness of sons. We then explain how multiple mating can elevate offspring fitness by increasing the number of potential sires that compete, when this occurs in conjunction with mechanisms of paternity biasing that function in copula or post-copulation. We begin by identifying cases where females use pre-copulatory cues to identify mates prior to remating. In the simplest case, females remate because they identify a superior mate and 'trade up' genetically. The main evidence for this process comes from extra-pair copulation in birds. Second, we note other cases where pre-copulatory cues may be less reliable and females mate with several males to promote post-copulatory mechanisms that bias paternity. Although a distinction is drawn between sperm competition and cryptic female choice, we point out that the genetic benefits to polyandry in terms of producing more viable or sexually attractive offspring do not depend on the exact mechanism that leads to biased paternity. Post-copulatory mechanisms of paternity biasing may: (1) reduce genetic incompatibility between male and female genetic contributions to offspring; (2) increase offspring viability if there is a positive correlation between traits favoured post-copulation and those that improve performance under natural selection; (3) increase the ability of sons to gain paternity when they mate with polyandrous females. A third possibility is that genetic diversity among offspring is directly favoured. This can be due to bet-hedging (due to mate assessment errors or temporal fluctuations in the environment), beneficial interactions between less related siblings or the opportunity to preferentially fertilise eggs with sperm of a specific genotype drawn from a range of stored sperm depending on prevailing environmental conditions. We use case studies from the social insects to provide some concrete examples of the role of genetic diversity among progeny in elevating fitness. We conclude that post-copulatory mechanisms provide a more reliable way of selecting a genetically compatible mate than pre-copulatory mate choice. Some of the best evidence for cryptic female choice by sperm selection is due to selection of more compatible sperm. Two future areas of research seem likely to be profitable. First, more experimental evidence is needed demonstrating that multiple mating increases offspring fitness via genetic gains. Second, the role of multiple mating in promoting assortative fertilization and increasing reproductive isolation between populations may help us to understand sympatric speciation.

Why do females mate multiply? A review of the genetic benefits.

Although there have been many molecular studies of morphological mutants generated in the laboratory, it is unclear how these are related to mutants in natural populations, where the constraints of natural selection and breeding structure are quite different. Here we characterize a naturally occurring mutant of Linaria vulgaris, originally described more than 250 years ago by Linnaeus, in which the fundamental symmetry of the flower is changed from bilateral to radial. We show that the mutant carries a defect in Lcyc, a homologue of the cycloidea gene which controls dorsoventral asymmetry in Antirrhinum. The Lcyc gene is extensively methylated and transcriptionally silent in the mutant. This modification is heritable and co-segregates with the mutant phenotype. Occasionally the mutant reverts phenotypically during somatic development, correlating with demethylation of Lcyc and restoration of gene expression. It is surprising that the first natural morphological mutant to be characterized should trace to methylation, given the rarity of this mutational mechanism in the laboratory. This indicates that epigenetic mutations may play a more significant role in evolution than has hitherto been suspected.

An epigenetic mutation responsible for natural variation in floral symmetry

Why do girls tend to earn better grades in school than boys? Why are men still far more likely than women to earn degrees in the fields of science, technology, engineering, and mathematics? And why are men on average more likely to be injured in accidents and fights than women? These and many other questions are the subject of both informal investigation in the media and formal investigation in academic and scientific circles. In his landmark book "Male, Female: The Evolution of Human Sex Differences", author David Geary provided the first comprehensive evolutionary model to explain human sex differences. Using the principles of sexual selection such as female choice and male-male competition, the author systematically reviewed and discussed the evolution of sex differences and their expression throughout the animal kingdom, as a means of not just describing but explaining the same process in Homo sapiens. Now, over ten years since the first edition, Geary has completed a massive update, expansion and theoretical revision of his classic text. New findings in brain and genetic research inform a wealth of new material, including a new chapter on sex differences in patterns of life history development; expanded coverage of genetic research (e.g. DNA finger printing to determine paternity as related to male-male competition in primates); fatherhood in humans; cross-cultural patterns of sex differences in choosing and competing for mates; and, genetic, hormonal, and socio-cultural influences on the expression of sex differences. Finally, through his motivation to control framework (introduction in the first edition and expanded in "The Origin of Mind", 2005), Geary presents a theoretical bridge linking parenting, mate choices, and competition, with children's development and sex differences in brain and cognition. The result is an even better book than the original - a lively and nuanced application of Darwin's insight to help explain our heritage and our place in the natural world.

Male, Female: The Evolution of Human Sex Differences

The phenomenon of inbreeding depression is well documented and behavioral adaptations for inbreeding avoidance have been described. However, there is debate over whether inbreeding depression is always an important selective force on behavior. Here, we summarize recent evidence for inbreeding depression under natural conditions, review inbreeding avoidance mechanisms, and discuss how these are influenced by social structure. We also examine the idea that animals have evolved mechanisms to avoid outbreeding.

Inbreeding avoidance in animals.

There is growing interest in the possibility that genetic compatibility may drive mate choice, including gamete choice, particularly from the perspective of understanding why females frequently mate with more than one male. Mate choice for compatibility differs from other forms of choice for genetic benefits (such as ‘good genes’) because individuals are expected to differ in their mate preferences, changing the evolutionary dynamics of sexual selection. Recent experiments designed to investigate genetic benefits of polyandry suggest that mate choice on the basis of genetic compatibility may be widespread. However, in most systems the mechanisms responsible for variation in compatibility are unknown. We review potential sources of variation in genetic compatibility and whether there is any evidence for mate choice driven by these factors. Selfish genetic elements appear to have the potential to drive mate compatibility mate choice, though as yet there is only one convincing example. There is abundant evidence for assortative mating between populations in hybrid zones, but very few examples where this is clearly a result of selection against mating with genetically less compatible individuals. There are also numerous cases of inbreeding avoidance, but little evidence that mate choice or differential fertilization success driven by genetic compatibility occurs between unrelated individuals. The exceptions to this are a handful of situations where both the alleles causing incompatibility and the alleles involved in mate choice are located in a chromosome region where recombination is suppressed. As yet there are only a few potential sources of genetic compatibility which have clearly been shown to drive mate choice. This may reflect limitations in the potential for the evolution of mate choice for genetic compatibility within populations, although the most promising sources of such incompatibilities have received relatively little research.

http://www.selfishgene.org/Tom/Papers/TTNW_MolEcol00.pdf

Genetic compatibility, mate choice and patterns of parentage: invited review.

Because of the central role of major histocompatibility complex (MHC) genes in immune recognition, it is often assumed that parasite-driven selection maintains the unprecendented genetic diversity of these genes. But associations between MHC genotype and specific infectious diseases have been difficult to identify with a few exceptions such as Marek's disease and malaria. Alternatively, MHC-related reproductive mechanisms such as selective abortion and mating preferences could be responsible for the diversity. To determine both the nature and strength of selection operating on MHC genes by we have studied components of selection in seminatural populations of mice (Mus musculus domesticus). Here we assess MHC-related patterns of reproduction and early (preweaning) mortality by analysing 1,139 progeny born in nine populations, and 662 progeny from laboratory matings. Reproductive mechanisms, primarily mating preferences, result in 27% fewer MHC-homozygous offspring than expected from random mating. MHC genotype had no detectable influence on neonatal (preweaning) mortality. These mating preferences are strong enough to account for most of the MHC genetic diversity found in natural populations of Mus.

Mating patterns in seminatural populations of mice influenced by MHC genotype.

Discovering the forces that maintain the extreme polymorphisms found at loci within the major histocompatibility complex (MHC) is critical to understanding the role of MHC gene products in nature. It is often assumed that MHC polymorphisms are maintained in natural populations by heterozygote advantage. The feasibility of this assumption is examined by applying population genetics models developed by Sewall Wright to relevant parameters for the MHC of Mus musculus (H-2). The parameters that affect the number of alleles that can be maintained (assuming random mating) are effective population size (Ne), mutation rate (p), and the selection against homozygotes relative to heterozygotes (s). The number of alleles that can be maintained for various combinations of Ne, p, and s are presented graphically. Even with extreme parameter values maximizing the number of alleles at equilibrium (Ne=100, p=10−4, s=1) only about seven alleles can be maintained within local populations. More commonly accepted sets of parameters indicate that heterozygote advantage could only account for the maintenance of four to five alleles. An analysis of previously published data suggest that local populations carry approximately ten alleles at both the K and D loci. These results indicate that either our estimates of the relevant parameters and number of alleles actually maintained contain significant errors, or that factors other than heterozygote advantage contribute to the maintenance of H-2 polymorphisms. We briefly review a number of mechanisms other than heterozygote advantage that could play a role in the maintenance of MHC polymorphisms, including frequency dependent selection, variation in pathogen assemblages across space and time, mating preferences, and transmission distortion. We present data from a retrospective analysis of backcross and F2 matings made during the early development of H-2 homozygous lines that show transmission distortion leading to a 52% deficiency of H-2 homozygotes (n=80, p<.002). This level of transmission distortion would contribute significantly to the maintenance of H-2 polymorphisms.

Can Heterozygote Advantage Account for the Maintenance of H-2 Polymorphisms

Sexual selection and MHC genes

Communal nesting and communal nursing in house mice, Mus musculus domesticus

It has been convincingly demonstrated that mice can discriminate MHC-related odors among congenic strains under laboratory conditions (see Yamaguchi et al. 1981). There is, however, debate about the use of these MHC-related odors as mate choice cues (Partridge, 1988; Klein et al., 1990; Nei and Hughes, 1991). MHC-based mate choice has been postulated to function either to produce presumably more fit MHC heterozygous offspring (Doherty and Zinkernagel, 1975) or to avoid close inbreeding (Brown, 1983). In either case, mating should be disassortative. Data from semi-natural half-wild enclosure studies (Potts et al., 1991) suggest that disassortative matings produce an excess (from random mating expectations) of MHC heterozygous progeny. Behavioral observations also suggest that these disassortative matings are due primarily to female choice. In a subset of 305 pups of known maternity, those in litters of mixed paternity (30 out of 58 litters) show a significant excess of heterozygotes over what would have been produced if females had mated only with their territorial males. Those litters sired only by the female’s territorial male did not deviate from the number of heterozygotes expected. This suggests that an important factor in producing more MHC heterozygous progeny is extra-territorial matings. In 41 observations of mating pairs, all matings took place on the territory of the male. All 13 extra-pair matings observed involved females who had left their nesting territory to travel to the territory of the male with which they were mating. No male was ever observed mating off of his territory. For details see Potts et al. this volume.

What’s Wrong with MHC Mate Choice Experiments?

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