Measuring Pre- and Post-Copulatory Sexual Selection and Their Interaction in Socially Monogamous Species with Extra-Pair Paternity

Abstract

When females copulate with multiple males, pre- and post-copulatory sexual selection may interact synergistically or in opposition. Studying this interaction in wild populations is complex and potentially biased, because copulation and fertilization success are often inferred from offspring parentage rather than being directly measured. Here, I simulated 15 species of socially monogamous birds with varying levels of extra-pair paternity, where I could independently cause a male secondary sexual trait to improve copulation success, and a sperm trait to improve fertilization success. By varying the degree of correlation between the male and sperm traits, I show that several common statistical approaches, including univariate selection gradients and paired t-tests comparing extra-pair males to the within-pair males they cuckolded, can give highly biased results for sperm traits. These tests should therefore be avoided for sperm traits in socially monogamous species with extra-pair paternity, unless the sperm trait is known to be uncorrelated with male trait(s) impacting copulation success. In contrast, multivariate selection analysis and a regression of the proportion of extra-pair brood(s) sired on the sperm trait of the extra-pair male (including only broods where the male sired ≥1 extra-pair offspring) were unbiased, and appear likely to be unbiased under a broad range of conditions for this mating system. In addition, I investigated whether the occurrence of pre-copulatory selection impacted the strength of post-copulatory selection, and vice versa. I found no evidence of an interaction under the conditions simulated, where the male trait impacted only copulation success and the sperm trait impacted only fertilization success. Instead, direct selection on each trait was independent of whether the other trait was under selection. Although pre- and post-copulatory selection strength was independent, selection on the two traits was positively correlated across species because selection on both traits increased with the frequency of extra-pair copulations in these socially monogamous species.

Sperm Numbers as a Paternity Guard in a Wild Bird

“…First, the opportunity for selection may be greater in some species than others [ 47 ], and indeed, in the two species in which a relationship between sperm traits and paternity success has been reported, extra-pair mating is common and subsequent rates of EPP are high ([ 43 , 44 ], reviewed in [ 47 ]). Second, a recent simulation study demonstrated that the use of parentage data to infer selection on sperm traits can lead to highly biased results under many common statistical approaches, especially when traits linked to pre-copulatory sexual selection are not taken into account [ 49 ]. Additionally, we suggest that it can be informative to take into account extrinsic ecological factors that may constrain the ability of individuals to engage in extra-pair mating.…”

Sperm length divergence as a potential prezygotic barrier in a passerine hybrid zone

“…Indeed, a high proportion of intermediate males sire no offspring (81% of 33 intermediate males, compared to 60% of 213 pure and back‐crossed males of both species in Walsh, Maxwell et al., 2018; or 53% of 17 intermediate males, compared to 25% of 103 pure and back‐crossed males of both species in Maxwell, 2018), although the number of offspring sired by successful intermediate males is similar to Nelson's sparrows (Maxwell, 2018; Walsh, Maxwell et al., 2018). Together, these observations may suggest that intermediate males suffer reduced copulation success but not reduced fertilization success following copulation, although disentangling pre‐ and postcopulatory processes using parentage data is challenging (Cramer, 2021).…”

“…For species with substantial sexual selection at both the pre‐ and postcopulatory stages, correlations between male traits promoting copulation success and sperm traits promoting fertilization success may have important consequences for trait evolution (Polak et al., 2021; Simmons et al., 2017), as well as for our ability to study it (Cramer, 2021). While this idea has been raised in many intraspecific studies, the relationships between pre‐ and postcopulatory traits that act as reproductive barriers are not well studied in hybrid zones.…”

“…Intermediate males are hypothesized to be at a disadvantage in courtship, being too large for the aerial acrobatics typical of Nelson's sparrows and too small for successful scramble competition against saltmarsh sparrows (Walsh, Maxwell et al, 2018 Maxwell, 2018), although the number of offspring sired by successful intermediate males is similar to Nelson's sparrows (Maxwell, 2018;Walsh, Maxwell et al, 2018). Together, these observations may suggest that intermediate males suffer reduced copulation success but not reduced fertilization success following copulation, although disentangling pre-and postcopulatory processes using parentage data is challenging (Cramer, 2021).…”

“…However, because male–female interactions are brief and the species are not territorial (Shriver et al., 2010), inferences of assortative mating are based on the genetic parentage of offspring rather than direct observations (Walsh, Maxwell et al., 2018). Inferring copulation patterns from parentage data is, however, not straightforward for species with sperm competition, since genetic parentage depends on successful fertilization of eggs as well as on copulations (Cramer, 2021). Further work is therefore needed to understand whether sperm and female reproductive phenotypes have also diverged, since poor sperm performance following heterospecific copulation can cause reproductive barriers between species (Howard et al., 2009).…”