Paternal Genetic Effects on Offspring Fitness Are Context Dependent: Within the Extrapair Mating System of a Socially: Monogamous Passerine

Abstract

Abstract. Avian extrapair mating systems provide an interesting model to assess the role of genetic benefits in the evolution of female multiple mating behavior, as potentially confounding nongenetic benefits of extrapair mate choice are seen to be of minor importance. Genetic benefit models of extrapair mating behavior predict that females engage in extrapair copulations with males of higher genetic quality compared to their social mates, thereby improving offspring reproductive value. The most straightforward test of such good genes models of extrapair mating implies pairwise comparisons of maternal half-siblings raised in the same environment, which permits direct assessment of paternal genetic effects on offspring traits. But genetic benefits of mate choice may be difficult to detect. Furthermore, the extent of genetic benefits (in terms of increased offspring viability or fecundity) may depend on the environmental context such that the proposed differences between extrapair offspring (EPO) and within-pair offspring (WPO) only appear under comparatively poor environmental conditions. We tested the hypothesis that genetic benefits of female extrapair mate choice are context dependent by analyzing offspring fitness-related traits in the coal tit (Parus ater) in relation to seasonal variation in environmental conditions. Paternal genetic effects on offspring fitness were context dependent, as shown by a significant interaction effect of differential paternal genetic contribution and offspring hatching date. EPO showed a higher local recruitment probability than their maternal half-siblings if born comparatively late in the season (i.e., when overall performance had significantly declined), while WPO performed better early in the season. The same general pattern of context dependence was evident when using the number of grandchildren born to a cuckolding female via her female WPO or EPO progeny as the respective fitness measure. However, we were unable to demonstrate that cuckolding females obtained a general genetic fitness benefit from extrapair fertilizations in terms of offspring viability or fecundity. Thus, another type of benefit could be responsible for maintaining female extrapair mating preferences in the study population. Our results suggest that more than a single selective pressure may have shaped the evolution of female extrapair mating behavior in socially monogamous passerines.

Sex-specific differential survival of extra-pair and within-pair offspring in song sparrows,Melospiza melodia

“…However, the relative survival of EPY and WPY and therefore the fitness consequences of EPP for females did not vary with season. By contrast, the only other study system where differential survival of EPY and WPY in early versus late broods was estimated showed that coal tit EPY had higher recruitment if hatched late in the season but tended to have lower recruitment if hatched early in the season, with no average effect of extra-pair status across all broods [34]. If anything, EPY on Mandarte tended to be less likely to survive from ringing to recruitment if hatched late in the season (table 1).…”

“…Indeed, any increased fitness of EPY has been predicted to be primarily manifested under poor conditions, such as late in the breeding season [33–35]. Since such sex- or environment-specific variation may alter the magnitude of any overall indirect benefit of extra-pair reproduction [32,34,36], rigorous studies comparing fitness components between EPY and WPY should explicitly quantify sex- and environment-specific effects.…”

Differences in perceived predation risk associated with variation in relative size of extra‐pair and within‐pair offspring

“…This idea has only formally been tested a handful of times, but these early studies have proved promising (Schmoll, ). In coal tits ( Periparus ater ), EPO were more likely to recruit into the breeding population than were WPO, but only if they had been born late in the season when overall breeding performance had declined (Schmoll et al, ). Likewise, common yellowthroat ( Geothlypis trichas ) EPO exhibited a stronger T‐cell‐mediated immune response than WPO only in the colder of two study years (Garvin, Abroe, Pedersen, Dunn, & Whittingham, ).…”

Superiority of extra-pair offspring: maternal but not genetic effects as revealed by a mixed cross-fostering design

“…Three factors might have caused problems with the estimation of indirect benefits to date. First, genetic effects might be context dependent and thus manifested only under some environmental conditions (Sheldon 2000a; Schmoll et al. 2005; Garvin et al.…”