Understanding why females mate with different partners within a single reproductive episode is not trivial. Polyandry enables intra- and intersexual selection to continue after mating in the form of sperm competition and/or cryptic female choice (reviewed in Parker 1970; Smith 1984; Eberhard 1996; Birkhead and Møller 1998; Simmons 2001). In addition, this behavior facilitates antagonistic interactions between the sexes if selection imposed by sperm competition drives the evolution of traits that increase the fitness of males at the expense of female fitness (Parker 1979; Johnstone and Keller 2000; Arnqvist and Rowe 2005). Traditional theory dictates that females should be reluctant to accept multiple partners due to asymmetries between the sexes in gamete size and provisioning of the zygote (Trivers 1972; Parker 1979), and evidence that mating can incur costs for females (Daly 1978; Rolff and Siva-Jothy 2002) supports the argument that polyandry should not be widespread. Nevertheless, females of many species mate polyandrously (Birkhead and Møller 1998; Jennions and Petrie 2000) and it has been proposed that this behavior can be explained if females accrue material or genetic benefits, or if males impose higher-than-optimal remating rates in females (Arnqvist and Nilsson 2000; Jennions and Petrie 2000; Arnqvist and Rowe 2005).
A series of genetic benefits has been suggested to increase fitness of polyandrous females (Yasui 1998; Jennions and Petrie 2000). Explanations based on intrinsic male quality propose that females can increase the probability that their eggs are fertilized by males of superior genetic quality, either through precopulatory or postcopulatory mechanisms (Kempenaers et al. 1992; Andersson 1994; Petrie 1994; Yasui 1997; Welch et al. 1998; Møller and Alatalo 1999; Jennions and Petrie 2000; Kokko et al. 2003; García-González and Simmons 2005a). Alternatively, multiple mated females can increase fitness by allowing male-by-female genetic incompatibilities to be resolved either before or after the fusion of the gametes (Zeh and Zeh 1997; Tregenza and Wedell 2000, 2002; Neff and Pitcher 2005). Experiments that manipulate the number of partners while controlling for mating frequency have supported genetic models based on the existence of postcopulatory phenomena: a meta-analysis of data arising from these studies shows that embryo viability, estimated as egg hatching success, is significantly enhanced in polyandrous matings (Simmons 2005). However, distinguishing whether these benefits are genetically based, and whether they arise because of fertilization biases due to intrinsic male genetic quality or due to interactions between parental genotypes is often not straightforward (Simmons 2005).
The postcopulatory analogy of the good genes model for female choice evolution, the good-sperm hypothesis (Yasui 1997), suggests that polyandrous females will accrue genetic quality for their offspring through facilitation of sperm competition if males achieving higher fertilization success are also more effective in producing viable offspring (Sivinski 1984; Parker 1992; Birkhead et al. 1993; Yasui 1997, 1998). The good-sperm model requires heritable variation among males in their general viability or condition (genetic quality), a premise for which there is little doubt (e.g., Houle 1992; Rowe and Houle 1996; Kokko 1998; Lynch and Walsh 1998; Welch et al. 1998; Wedekind et al. 2001; Sheldon et al. 2003; Hunt et al. 2004; Tomkins et al. 2004). In addition, the model assumes that the outcome of sperm competition is determined by the males' investment in sperm competition, and that males exhibit intrinsic differences in their ability to invest in sperm competitiveness. A large body of literature on sperm competition shows that even though females play an active role in the output of sperm competition (Wilson et al. 1997; Clark and Begun 1998; Clark et al. 1999; Clark 2002; Miller and Pitnick 2002; García-González and Simmons 2007b), fertilization success is often determined by ejaculate traits, sperm traits, or male genital morphology in a broad range of taxa including birds, mammals, fish and insects (Birkhead and Møller 1998; Hosken and Stockley 2004; Snook 2005; Evans and Simmons 2008; Simmons and Moore 2008). Importantly, although the inheritance of male traits that determine fertilization success may be constrained, for example by sex linkage or cytoplasmic genetic effects (Birkhead and Pizzari 2002; Pizzari and Birkhead 2002; Zeh 2004; Froman and Kirby 2005; Zeh and Zeh 2008), a wealth of research suggests that, at least in some species, traits contributing to fertilization success can be explained by intrinsic differences among males (e.g., Dziuk 1996; Radwan 1998; Konior et al. 2006). Furthermore, some recent studies implicate male condition dependence on investment in sperm competition traits in some taxa (e.g., Hosken et al. 2001; Simmons and Kotiaho 2002; Engqvist and Sauer 2003; Schulte-Hostedde et al. 2005; and see review by Simmons and Moore 2008). Thus, at least in some systems, the assumptions of the good-sperm model are supported. Furthermore, accumulating evidence from studies with increased power to detect intrinsic sire effects supports the notion that polyandry may increase the probability of fertilization by genetically superior males (García-González and Simmons 2005a; and see Evans and Simmons 2008). So far however, empirical support for the acquisition of offspring genetic quality through a good-sperm process is scant (Pai and Yan 2002; Hosken et al. 2003; Fisher et al. 2006; García-González and Simmons 2007b; Simmons and Kotiaho 2007), and only one study so far has found clear support for the fertilization success-offspring viability association predicted by the good-sperm model (Fisher et al. 2006).
In this article, I review an issue relating to sperm competition and male genetic quality that may affect the ability to detect and interpret underlying good-sperm processes. Recent verbal arguments point out that caution should be taken when estimating fertilization success because the assignment of paternity at late stages of offspring development can be confounded with mortality rates in embryos (e.g., Jennions and Petrie 2000; Birkhead et al. 2004; Simmons 2005; Evans et al. 2007; García-González and Simmons 2007a, and see below). It is useful to make the distinction between fertilization success sensu stricto, estimated at conception (referred to in this article as F2, or the proportion of eggs fertilized by the last male to mate a doubly mated female) from paternity success estimated at hatching or birth, typically P2, or the proportion of offspring sired by the second male to mate a doubly mated female (Boorman and Parker 1976). Because of methodological constraints, studies of postcopulatory sexual selection generally infer fertilization success (proxy for sperm competitive ability) from P2 values. However, paternity success measures are inescapably conditioned by the normal development of embryos from fertilization to hatching/birth. This begs the question of whether estimations of the ability of males to win fertilizations are confounded by differential embryo viability. Differential embryo viability across a female's mates can result from either intrinsic sire effects (García-González and Simmons 2005a; Ivy 2007), genetic incompatibilities between males and females (Olsson et al. 1999), differential allocation and maternal indirect genetic effects (Sheldon 2000; Tregenza et al. 2003), or paternal indirect genetic effects and interacting phenotypes (García-González and Simmons 2007a). Gilchrist and Partridge (1997) pioneering study showed that the apparent heritability of sperm competitiveness in Drosophila melanogaster was to a great degree explained by heritability of preadult viability. Later on, Olsson et al. (1999) highlighted that, in the context of cryptic female choice and genetic incompatibilities, parental relatedness may produce inbreeding-induced mortality that would introduce noise in paternity data. More recent studies indicate that the period between the onset of fertilization and hatching or birth is a critical stage in which differential embryo mortality across a female's mates occurs (Wedekind et al. 2001; García-González and Simmons 2007a; Evans and Simmons 2008). Studies examining good-sperm processes would typically look at the relationship between paternity success (P2) and post-hatching offspring viability (e.g., survival from juvenile to adult). This study examines the extent to which intrinsic sire effects on embryo viability can confound estimates of fertilization success when using paternity success data, and the consequences of these effects for the study of postcopulatory sexual selection, in particular for empirical tests of the good-sperm hypothesis.