Male "mixed" reproductive strategies in biparental species: Trivers was probably right, but why?

Trivers proposed that, if parental care by both sexes is advantageous, males should practice a "mixed" strategy of seeking extrapair copulations, while restricting their parental investment to offspring of social mates. We explore circumstances under which males should limit their parental care in the predicted manner. We find that Trivers's "mixed" strategy will generally be evolutionarily stable so long as either socially monogamous or polygynous males usually sire more offspring per brood from a social mate than they typically sire in broods of extrapair mates. Polygynous males should spread investment across their home nests unless the expected number of chicks sired in them differs widely. Whether polygynous males should restrict paternal care to social mates' offspring hinges additionally on resident male investment in broods containing extrapair young: if resident males contribute minimally, some investment by a polygynous extrapair male becomes more advantageous. Recently reviewed data on extrapair fertilization distributions within monogamous and polygynous passerines suggest that extrapair offspring often predominate numerically within their broods, consistent with sperm expenditure theory. Nevertheless, most species conform to the model's criterion regarding relative parentage levels in broods of social versus extrapair mates. Patterns of extrapair parentage thus appear sufficient to stabilize biparental care systems.

Parker GA ，Schwagmeyer PL 《-》

Paternal genetic effects on offspring fitness are context dependent within the extrapair mating system of a socially monogamous passerine.

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.

Schmoll T ，Dietrich V ，Winkel W ，Epplen JT ，Schurr F ，Lubjuhn T ... -  《EVOLUTION》

Multiple genetic benefits of female promiscuity in a socially monogamous passerine.

The adaptive function of female extrapair mating in socially monogamous passerines is currently debated. In the bluethroat (Luscinia s. svecica), a previous study showed that offspring sired by extrapair males had a higher cell-mediated immunity than their within-pair half siblings, suggesting an immunogenetic benefit of extrapair mating in this species. Here, we expanded that dataset with two more years and investigated the association between extrapair paternity and microsatellite multilocus heterozygosity, in addition to cell-mediated immunity. We found that extrapair offspring were more heterozygous than their within-pair half siblings, and corroborated the previous finding of enhanced cellular immunity in extrapair offspring in this four-year dataset. The increased heterozygosity among extrapair offspring appeared to be a result of extrapair mates being less genetically similar than pair mates, and also less genetically similar than expected by random choice. Together with previous findings in this species, showing that the majority of females participate in extrapair copulations, our results indicate a postcopulatory cryptic female choice of genetically dissimilar males. The enhanced cellular immunity and increased heterozygosity were not related to each other, and hence our results indicate two independent genetic benefits of extrapair mating in the bluethroat.

Fossøy F ，Johnsen A ，Lifjeld JT 《EVOLUTION》

Little effect of extrapair paternity on the opportunity for sexual selection in Savannah sparrows (Passerculus sandwichensis).

Extrapair paternity (EPP) can dramatically increase the opportunity for sexual selection if relatively few males are able to monopolize the majority of fertilizations in a population. Although recent work with birds suggests that EPP can increase the standardized variance in male reproductive success (Is) as much as 13-fold, only a male's within-pair success is typically quantified with any accuracy. In most cases, nearly half of all extrapair young are of unknown parentage. A strong, negative correlation across studies between the proportion of extrapair young for which parentage is known and the apparent effect of EPP on Is (r(s) = -0.71, P = 0.013, N = 13 studies) suggests that the incomplete sampling of extrapair sires has greatly exaggerated the influence of EPP. To achieve a more thorough accounting of EPP and its importance to variation in male fitness, we used a suite of four to six microsatellite loci to identify extrapair young and their sires in a polygynous population of Savannah sparrows (Passerculus sandwichensis). Pooling over the 2002 and 2003 breeding seasons, 79 of 116 females (68.1%) produced young outside of the pairbond and 194 of 411 offspring (47.2%) were extrapair. We identified sires for 96.4% of all young (N = 396), including sires for 92.3% of the extrapair young (N = 179), allowing us to partition Is into within-pair and extrapair components. In both years, EPP-related fitness components generated more variation in male reproductive success than the number or quality of within-pair mates. Differences among males in the number of extrapair mates alone accounted for 56.6% of Is in 2002 and for 23.6% of Is in 2003. Nonetheless, in absolute terms, the occurrence of EPP on Kent Island increased the opportunity for sexual selection less than two-fold. Averaging over the two years, Is was only 78% higher than Is,app, the variance in male reproductive success that would have occurred had EPP been nonexistent and males sired all young on their territories. Likewise, across nine socially monogamous species, we found no correlation between the extent of EPP and its effect on the opportunity for sexual selection (Is/Is,app) and only a marginally significant positive correlation between EPP and Is itself. Taken together, our results suggest that the relationship between EPP and sexual selection in birds may be much less strong and much less straightforward than commonly thought.

Freeman-Gallant CR ，Wheelwright NT ，Meiklejohn KE ，States SL ，Sollecito SV ... -  《EVOLUTION》

The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females.

Many studies have been aimed at understanding the maintenance of female infidelity in socially monogamous birds. Because engaging in extrapair copulations (EPCs) is believed to be costly for females, it has been argued that EPC behavior must bring indirect benefits to females by elevating offspring fitness. We use empirical data from the literature to assess the relative strength of indirect and direct selection on female EPC behavior, using quantitative genetic approximations of selection. This analysis confirmed that there is generally negative direct selection on EPC behavior caused by depressed paternal investment by social males. In contrast, there was no significant positive indirect selection on EPC behavior in females. A comparison between the two types of selection suggests that the force of direct negative selection is generally much stronger than that of indirect positive selection. Indirect selection is thus unlikely to maintain EPC behavior in the face of direct selection against it. We suggest that EPCs may instead be the result of antagonistic selection on loci influencing the outcome of male-female encounters and that EPC behavior per se may not be adaptive for females but may reflect sexual conflict due to strong selection in males to achieve extrapair copulations.

Arnqvist G ，Kirkpatrick M 《-》