Genetic quality and sexual selection: an integrated framework for good genes and compatible genes

Abstract

Why are females so choosy when it comes to mating? This question has puzzled and marveled evolutionary and behavioral ecologists for decades. In mating systems in which males provide direct benefits to the female or her offspring, such as food or shelter, the answer seems straightforward -females should prefer to mate with males that are able to provide more resources. The answer is less clear in other mating systems in which males provide no resources (other than sperm) to females. Theoretical models that account for the evolution of mate choice in such nonresource-based mating systems require that females obtain a genetic benefit through increased offspring fitness from their choice. Empirical studies of nonresourcebased mating systems that are characterized by strong female choice for males with elaborate sexual traits (like the large tail of peacocks) suggest that additive genetic benefits can explain only a small percentage of the variation in fitness. Other research on genetic benefits has examined nonadditive effects as another source of genetic variation in fitness and a potential benefit to female mate choice. In this paper, we review the sexual selection literature on genetic quality to address five objectives. First, we attempt to provide an integrated framework for discussing genetic quality. We propose that the term 'good gene' be used exclusively to refer to additive genetic variation in fitness, 'compatible gene' be used to refer to nonadditive genetic variation in fitness, and 'genetic quality' be defined as the sum of the two effects. Second, we review empirical approaches used to calculate the effect size of genetic quality and discuss these approaches in the context of measuring benefits from good genes, compatible genes and both types of genes. Third, we discuss biological mechanisms for acquiring and promoting offspring genetic quality and categorize these into three stages during breeding: (i) precopulatory (mate choice); (ii) postcopulatory, prefertilization (sperm utilization); and (iii) postcopulatory, postfertilization (differential investment). Fourth, we present a verbal model of the effect of good genes sexual selection and compatible genes sexual selection on population genetic variation in fitness, and discuss the potential trade-offs that might exist between mate choice for good genes and mate choice for compatible genes. Fifth, we discuss some future directions for research on genetic quality and sexual selection.

Promiscuous mating produces offspring with higher lifetime fitness

“…Although our data strongly suggest the presence of genetic indirect benefits, they do not allow us to distinguish between these two competing hypotheses. Such a test requires partitioning indirect benefits into additive and non-additive genetic components [38], which is not feasible given the low rate of return of nestlings to our population (10.4% of banded fledglings, which is typical of most songbirds).…”

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

“…Genetic benefits in the form of good or compatible genes for the offspring are still the prominent hypothesis for why females engage in extra-pair matings [3][4][5][6] (but see [7][8][9][10] for alternative explanations such as sexual conflict). In line with this hypothesis, a growing number of studies have demonstrated that extra-pair offspring (EPO) are superior to their within-pair half-sibs in a number of fitness-related traits [11 -16].…”

A distinct reed bunting dawn song and its relation to extrapair paternity

“…Second, within the female's reproductive tract, a subsequent cryptic female choice (Birkhead & Pizzari 2002) could take place, where sperm of 'good singers' are selected for compatibility. The relative importance of the two indirect genetic benefits may depend on the current genetic set-up of the population and change over time (Neff & Pitcher 2005). Whether she goes for compatible or for good genes may also depend on a female's genotype (Kempenaers 2007).…”

“…On the other hand, females may additionally profit through extrapair matings with compatible males that show elaborate song traits because they could get, at the same time, both good and compatible genes for their offspring. Benefits of extrapair fertilization can be based on both good and compatible genes, as they are not mutually exclusive (Neff & Pitcher 2005). Female choice could then be separated into two steps.…”