Tom Tregenza

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

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.

Sexual selection and speciation

The power of sexual selection to drive changes in mate recognition traits gives it the potential to be a potent force in speciation. Much of the evidence to support this possibility comes from comparative studies that examine differences in the number of species between clades that apparently differ in the intensity of sexual selection. We argue that more detailed studies are needed, examining extinction rates and other sources of variation in species richness. Typically, investigations of extant natural populations have been too indirect to convincingly conclude speciation by sexual selection. Recent empirical work, however, is beginning to take a more direct approach and rule out confounding variables.

Polyandrous females avoid costs of inbreeding

Why do females typically mate with more than one male? Female mating patterns have broad implications for sexual selection, speciation and conflicts of interest between the sexes, and yet they are poorly understood. Matings inevitably have costs, and for females, the benefits of taking more than one mate are rarely obvious. One possible explanation is that females gain benefits because they can avoid using sperm from genetically incompatible males, or invest less in the offspring of such males. It has been shown that mating with more than one male can increase offspring viability, but we present the first clear demonstration that this occurs because females with several mates avoid the negative effects of genetic incompatibility. We show that in crickets, the eggs of females that mate only with siblings have decreased hatching success. However, if females mate with both a sibling and a non-sibling they avoid altogether the low egg viability associated with sibling matings. If similar effects occur in other species, inbreeding avoidance may be important in understanding the prevalence of multiple mating.

Phylogenies and the Comparative Method in Animal Behaviour

1. Phylogenetics in behavior 2. The statistical analysis of interspecific data 3. How to study comparative methods for discrete characters 4. The mechanistic bases of behavioral evolution 5. Geographic variation in behavior 6. Phylogenetic liability and rates of phenotypic evolution 7. Comparing behavioral and morphological characters as indicators of phylogeny 8. The phylogenetic content of avian courtship display and song evolution 9. Comparative analysis of the origins and losses of eusociality 10. Using comparative approaches to integrate behavior and population biology 11. Phylogenetic interpretations of primate socioecology 12. Using cladistic analysis of comparative data to reconstruct the evolution of cognitive development in hominids

Sexual selection and animal personality

Consistent individual behavioural tendencies, termed “personalities”, have been identified in a wide range of animals. Functional explanations for personality have been proposed, but as yet, very little consideration has been given to a possible role for sexual selection in maintaining differences in personality and its stability within individuals. We provide an overview of the available literature on the role of personality traits in intrasexual competition and mate choice in both human and non‐human animals and integrate this into a framework for considering how sexual selection can generate and maintain personality. For this, we consider the evolution and maintenance of both main aspects of animal personality: inter‐individual variation and intra‐individual consistency.

Building on the Ideal Free Distribution

Publisher Summary This chapter reviews how the question of animal distributions has been approached from the point of view of individual behavior. The basis for much of the work on this subject has been the Ideal Free Distribution (IFD) theory, which considers that the suitability of any area of the environment is a function of the density of competitors occurring there. The chapter reviews how ideal free theory has been developed and examines whether the predictions of IFD models are supported by experimental and field studies. Furthermore, the assumptions of equal competitive ability, omniscience, movement without costs and a single type of competition have all be shown to be inappropriate in many situations. When unequal competitors are considered, a range of new distributions are predicted including phenotypes being truncated across patches of different quality. Lack of omniscience and costs to movement also affect predicted distributions, leading to a greater use of poorer patches, with the magnitude of this effect dependent on the composition of the environment. Therefore, several different forms of competition have been identified, and a corresponding range of models and predictions formulated.

BENEFITS OF MULTIPLE MATES IN THE CRICKET GRYLLUS BIMACULATUS

Despite the importance of polyandry for sexual selection, the reasons why females frequently mate with several males remain poorly understood. A number of genetic benefits have been proposed, based on the idea that by taking multiple mates, females increase the likelihood that their offspring will be sired by genetically more compatible or superior males. If certain males have intrinsically “good genes,” any female mating with them will produce superior offspring. Alternatively, if some males have genetic elements that are incompatible with a particular female, then she may benefit from polyandry if the sperm of such males are less likely to fertilize her eggs. We examined these hypotheses in the field cricket Gryllus bimaculatus (Orthoptera: Gryllidae). By allocating females identical numbers of matings but different numbers of mates we investigated the influence of number of mates on female fecundity, and both short‐ and long‐term offspring fitness. This revealed no effect of number of mates on number of eggs laid. However, hatching success of eggs increased with number of mates. This effect could not be attributed to nongenetic effects such as the possibility that polyandry reduces variance in the quantity or fertilizing ability of sperm females receive, because a control group receiving half the number of copulations showed no drop in hatching success. Offspring did not differ in survival, adult mass, size, or development time with treatment. When males were mated to several different females there were no repeatable differences between individual males in the hatching success of their mates eggs. This suggests that improved hatching success of polyandrous females is not due to certain males having genes that improve egg viability regardless of their mate. Instead, our results support the hypothesis that certain males are genetically more compatible with certain females, and that this drives polyandry through differential fertilization success of sperm from more compatible males.

Natural and Sexual Selection in a Wild Insect Population

Insects in the Wild Insects are of fundamental importance to terrestrial ecosystems and provide laboratory model systems for the study of physiology and genetics. Studies examining how natural and sexual selection operate to drive evolution in wild populations have often neglected invertebrates, resulting in a chasm between our understandings of how things work in the lab versus the natural environment. Rodríguez-Muñoz et al. (p. 1269; see the Perspective by Zuk) bridge this gap by comprehensively monitoring the life histories, behavior, and reproductive success of an entire population of field crickets. Adding genetic data allowed evaluation of how behavior impacts reproductive success and confirmed that male reproductive success varies more than that of females. Monitoring reproduction in wild crickets confirms that male success varies more than female success. The understanding of natural and sexual selection requires both field and laboratory studies to exploit the advantages and avoid the disadvantages of each approach. However, studies have tended to be polarized among the types of organisms studied, with vertebrates studied in the field and invertebrates in the lab. We used video monitoring combined with DNA profiling of all of the members of a wild population of field crickets across two generations to capture the factors predicting the reproductive success of males and females. The factors that predict a male’s success in gaining mates differ from those that predict how many offspring he has. We confirm the fundamental prediction that males vary more in their reproductive success than females, and we find that females as well as males leave more offspring when they mate with more partners.

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

Female promiscuity has broad implications for individual behaviour, population genetics and even speciation. In the field cricket Gryllus bimaculatus, females will mate with almost any male presented to them, despite receiving no recorded direct benefits. Previous studies have shown that female crickets can benefit from polyandry through increased hatching success of their eggs. There is evidence that this effect is driven by the potential of polyandrous females to avoid fertilizing eggs with sperm from genetically incompatible males. We provide direct evidence supporting the hypothesis that polyandry is a mechanism to avoid genetic incompatibilities resulting from inbreeding. Using microsatellite markers we examined patterns of paternity in an experiment where each female mated with both a related and an unrelated male in either order. Overall, unrelated males were more successful in gaining paternity than were related males, but this effect was driven by a much greater success of unrelated males when they were the first to mate.

SUCCESSFUL FATHERS SIRE SUCCESSFUL SONS

The theory of sexual selection holds a central role in evolutionary biology. Its key assumption is the heritability of traits associated with reproductive success. Strong indirect evidence supporting this assumption comes from the numerous studies that have identified heritable traits associated with mating success. However, there remain only a handful of studies that have attempted to demonstrate directly that successful fathers have successful sons. We present the results of an experimental study of the mating success and phenotype of male field crickets Gryllus bimaculatus (Orthoptera: Gryllidae) and their offspring. These reveal that sons of successful males obtain significantly more copulations than sons of unsuccessful males. There was no difference in body size of sons of either group, but sons of successful males had significantly longer development times. This may represent a naturally selected cost to traits associated with success that could balance their sexually selected advantages.