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

Abstract

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 be...

Increased heterozygosity for MHC class II lineages in newborn males

“…Recent studies suggested that genetic benefits drive not only pre-copulatory but also post-copulatory female choice in animals. 11,33,34 Genetic compatibility is more easily detected post-copulation via signals on sperm, and sperm-soma or egg-sperm interactions. 34 No other study has sought evidence for MHCmediated prenatal selection in newborns despite that this is an expected consequence of various observations regarding the influence of the MHC on reproductive physiology.…”

Same school, different conduct: rates of multiple paternity vary within a mixed‐species breeding school of semi‐pelagic cichlid fish (Cyprichromisspp.)

“…Alternative sources of variation are related to species‐specific reproductive, demographic or behavioral traits. For instance, clutch size can contribute to multiple paternity rates, particularly in the context of bet‐hedging (Jennions and Petrie 2000), but there was no significant difference in brood size between the two Cyprichromis species. A more likely source of mating pattern variation are potential between‐species differences in the densities of males and females within the school, which can influence mating patterns (Reichard et al.…”

“…Multiple paternity can also reflect females seeking benefits from mating with more than one male (Arnqvist and Nilsson 2000; Jennions and Petrie 2000; Taylor et al. 2014).…”

“…Females often do not stand to gain any material benefits from mating with multiple males during a single reproductive cycle, but genetic benefits may arise that outweigh the costs of polyandry. For example, females may “trade up” by remating upon encountering higher quality males after an initial mating event, exercise postcopulatory choice by preferentially increasing the fertilization success of certain sperm, or reap the benefits of a bet‐hedging strategy which aims to increase offspring fitness via increased genetic diversity within broods (Arnqvist and Nilsson 2000; Jennions and Petrie 2000). Even alternative male reproductive tactics such as “sneaking,” which have generally been viewed as harmful to female fitness as they undermine female mate choice, may provide benefits to females in some circumstances (Reichard et al.…”

Sexual Conflict Arising from Extrapair Matings in Birds

“…More specifically, it raised the questions as to why females would pursue and benefit from matings outside the social pair bond (Westneat et al 1990;Petrie and Kempenaers 1998), and why a female would benefit from mating with more than one male for a given clutch or litter. This new focus on females brought attention to the issue of polyandry more generally (Jennions and Petrie 2000;Simmons 2005;Parker and Birkhead 2013;Pizzari and Wedell 2013).…”