Experimental food supplementation reveals habitat-dependent male reproductive investment in a migratory bird.
ABSTRACT: Environmental factors can shape reproductive investment strategies and influence the variance in male mating success. Environmental effects on extrapair paternity have traditionally been ascribed to aspects of the social environment, such as breeding density and synchrony. However, social factors are often confounded with habitat quality and are challenging to disentangle. We used both natural variation in habitat quality and a food supplementation experiment to separate the effects of food availability-one key aspect of habitat quality-on extrapair paternity (EPP) and reproductive success in the black-throated blue warbler, Setophaga caerulescens. High natural food availability was associated with higher within-pair paternity (WPP) and fledging two broods late in the breeding season, but lower EPP. Food-supplemented males had higher WPP leading to higher reproductive success relative to controls, and when in low-quality habitat, food-supplemented males were more likely to fledge two broods but less likely to gain EPP. Our results demonstrate that food availability affects trade-offs in reproductive activities. When food constraints are reduced, males invest in WPP at the expense of EPP. These findings imply that environmental change could alter how individuals allocate their resources and affect the selective environment that drives variation in male mating success.
Project description:Many studies investigated variation in the frequency of extrapair paternity (EPP) among individuals. However, our understanding of within-individual variation in EPP remains limited. Here, we comprehensively investigate variation in EPP at the within-individual level in a population of blue tits (<i>Cyanistes caeruleus</i>). Our study is based on parentage data comprising >10 000 genotyped offspring across 11 breeding seasons. First, we examined the repeatability of the occurrence of EPP, the number of extrapair offspring, the number of extrapair partners, and the occurrence of paternity loss using data from males and females that bred in multiple years. Second, we tested whether within-individual changes in EPP between breeding seasons relate to between-year changes in the local social environment. Repeatabilities were generally low but significant for the occurrence and number of extrapair young in females and for whether a male sired extrapair young or not. We found no evidence that the presence of the former social partner or changes in the proportion of familiar individuals or in phenotypic traits of the neighbors influenced changes in levels of EPP in females. However, in adult males, a decrease in the average body size of male neighbors was associated with higher extrapair siring success. If confirmed, this result suggests that the competitive ability of a male relative to its neighbors influences his extrapair mating success. We suggest that alternative hypotheses, including the idea that within-individual changes in EPP are due to "chance events" rather than changes in an individual's social breeding environment, deserve more consideration.
Project description:In most cooperative breeders, helping is directed at close kin, allowing helpers to gain indirect fitness benefits by increasing the reproductive success of close relatives, usually their parents. Extrapair paternity (EPP) occurs at high rates in some cooperative breeders, reducing the relatedness of helpers to the young they help raise. Even so, a son that helps is related to the brood by at least 0.25 through his mother and to within-pair young by 0.5, whereas a potential helper that has EPP in his own nest is related only to the offspring he sires and unrelated to any extrapair offspring. In birds, EPP often favors older males, which in the extreme case can result in sons being more closely related to young in their parents' nest than to young in their own nests. The fitness benefit of helping will thus be enhanced if helping lightens the workload and increases survival of helpers and their fathers, enabling them to become old, hyper-successful extrapair sires. Here, we develop and analyze a proof-of-concept model, grounded in the western bluebird (<i>Sialia mexicana</i>) system, demonstrating the conditions under which high population levels of EPP can generate inclusive fitness benefits of helping behavior that outweigh the costs. This model provides a new perspective on the relationship between EPP and helping behavior in cooperative breeders and suggests a strong need for empirical work to gather unprecedented data on paternity over the lifetime of helpers and their parents.
Project description:Extrapair mating could drive sexual selection in socially monogamous species, but support for this hypothesis remains equivocal. We used lifetime fitness data and a unique model species, the dimorphic white-throated sparrow (Zonotrichia albicollis), to examine how extrapair mating affects the potential for sexual selection. In this species, the morphs employ distinct reproductive strategies, with white males pursuing extrapair mating at higher rates than tan counterparts. Social and extrapair mating is disassortative by morph, with paternity exchange occurring primarily between pairs composed of white males and tan females. Bateman gradients and Jones indexes indicated stronger sexual selection via mate numbers in white males than in females and tan males, and generally did not differ between females as compared with tan males. Extrapair mating contributed more to the Bateman gradient for white than tan males, and white males also had higher variance in annual reproductive success. However, variance in lifetime reproductive success did not differ between morphs or sexes. Moreover, extrapair mating did not increase variance in male reproductive success relative to apparent patterns, and within-pair success accounted for much more variance than extrapair success. Thus, extrapair mating by white males increases Bateman gradients and the potential for sexual selection via mate numbers. However, our latter results support previous research suggesting that extrapair mating may play a limited role in driving the overall potential for sexual selection.
Project description:Among nonhuman species, social monogamy is rarely accompanied by complete fidelity. Evolutionary theory predicts that the rate of extrapair paternity (EPP) should vary according to socioecological conditions. In humans, however, geneticists contend that EPP is negligible and relatively invariable. This conclusion is based on a limited set of studies, almost all of which describe European-descent groups. Using a novel, double-blind method designed in collaboration with a community of Himba pastoralists, we find that the rate of EPP in this population is 48%, with 70% of couples having at least one EPP child. Both men and women were very accurate at detecting cases of EPP. These data suggest that the range of variation in EPP across human populations is substantially greater than previously thought. We further show that a high rate of EPP can be accompanied by high paternity confidence, which highlights the importance of disaggregating EPP from the notion of “cuckoldry.”
Project description:Molecular techniques have revealed striking variation among bird species in the rates of extra-pair paternity (EPP) and intraspecific brood parasitism (IBP). In terms of the proportion of broods affected, rates of EPP and IBP vary across species from 0-95% and 0-50%, respectively. Despite a plethora of hypotheses and several careful comparative analyses, few robust correlates of this interspecific variation have been identified. One explanation for this shortfall is that most comparative studies have tended to focus on contemporary ecological factors and ignored fundamental differences in reproductive biology that evolved millions of years ago. We show that, for both EPP and IBP, over 50% of interspecific variation is due to differences among taxonomic families and orders. Therefore, we test hypotheses that predict interspecific variation in the rate of alternative reproductive strategies should be associated with differences in life history and the form of parental care. Our analyses largely support these predictions, with high rates of reproductive cheating being associated with 'fast' life histories. High EPP rates are associated with high rates of adult mortality and reduced paternal care. High IBP rates are associated with high-fecundity rates. These patterns remain intact whether we use species as independent data points or evolutionary contrasts based on either molecular or morphological phylogenies. These results are interpreted as supporting the idea that alternative reproductive strategies are most common in taxa in which the risks of retaliation are low. We suggest a hierarchical explanation for interspecific variation in the incidence of alternative reproductive strategies. Variation between major avian lineages in the EPP and IBP rates are determined by fundamental differences in life history and parental care that evolved many millions of years ago. Variation between populations or individuals of the same species, however, are more likely to be determined by differences in contemporary ecological and genetic factors.
Project description:The reduction in fecundity associated with the evolution of viviparity may have far-reaching implications for the ecology, demography, and evolution of populations. The evolution of a polygamous behaviour (e.g. polyandry) may counteract some of the effects underlying a lower fecundity, such as the reduction in genetic diversity. Comparing patterns of multiple paternity between reproductive modes allows us to understand how viviparity accounts for the trade-off between offspring quality and quantity. We analysed genetic patterns of paternity and offspring genetic diversity across 42 families from two modes of viviparity in a reproductive polymorphic species, Salamandra salamandra. This species shows an ancestral (larviparity: large clutches of free aquatic larvae), and a derived reproductive mode (pueriparity: smaller clutches of larger terrestrial juveniles). Our results confirm the existence of multiple paternity in pueriparous salamanders. Furthermore, we show the evolution of pueriparity maintains, and even increases, the occurrence of multiple paternity and the number of sires compared to larviparity, though we did not find a clear effect on genetic diversity. High incidence of multiple paternity in pueriparous populations might arise as a mechanism to avoid fertilization failures and to ensure reproductive success, and thus has important implications in highly isolated populations with small broods.
Project description:Extra-pair paternity (EPP) has been suggested to improve the genetic quality of offspring, but evidence has been equivocal. Benefits of EPP may be only available to specific individuals or under certain conditions. Red-winged fairy-wrens have extremely high levels of EPP, suggesting fitness benefits might be large and available to most individuals. Furthermore, extreme philopatry commonly leads to incestuous social pairings, so inbreeding avoidance may be an important selection pressure. Here, we quantified the fitness benefits of EPP under varying conditions and across life-stages. Extra-pair offspring (EPO) did not appear to have higher fitness than within-pair offspring (WPO), neither in poor years nor in the absence of helpers-at-the-nest. However, EPP was beneficial for closely related social pairs, because inbred WPO suffered an overall 75% reduction in fitness. Inbreeding depression was nonlinear and reduced nestling body condition, first year survival and reproductive success. Our comprehensive study indicates that EPP should be favored for the 17% of females paired incestuously, but cannot explain the widespread infidelity in this species. Furthermore, our finding that fitness benefits of EPP only become apparent for a small part of the population could potentially explain the apparent absence of fitness differences in population wide comparisons of EPO and WPO.
Project description:When mates are limited, individuals should allocate resources to mating tactics that maximize fitness. In species with extra-pair paternity (EPP), males can invest in mate guarding, or, alternatively, in seeking EPP. Males should optimize fitness by adjusting investment according to their attractiveness to females, such that attractive males seek EPP, and unattractive males guard mates. This theory has received little empirical testing, leaving our understanding of the evolution of mating tactics incomplete; it is unclear how a male's relative attractiveness influences his tactics. We conducted observations and experiments on red-backed fairy-wrens (Malurus melanocephalus) to address this question. We found that older, more attractive (red-black) males sought EPP, whereas unattractive (brown) males invested in alternative tactics-physical and acoustic mate guarding. Younger red-black males used intermediate tactics. This suggests that males adopt mating tactics appropriate to their attributes. Males obtained similar reproductive success, suggesting these alternative tactics may maximize each male's paternity gain. Though it is likely that female choice also determines paternity, rather than just male tactics, we establish that the many interconnected components of a male's sexual phenotype influence the evolution of his decision-making rules, deepening our understanding of how mating tactics evolve under sexual selection.
Project description:BACKGROUND: Polyandry is a common mating strategy in animals, increasing female fitness through direct (material) and indirect (genetic) benefits. Most theories about the benefits of polyandry come from studies of terrestrial animals, which have relatively complex mating systems and behaviors; less is known about the potential benefits of polyandry in sessile marine animals, for which potential mates may be scarce and females have less control over pre-copulatory mate choice. Here, we used microsatellite markers to examine multiple paternity in natural aggregations of the Pacific gooseneck barnacle Pollicipes elegans, testing the effect of density on paternity and mate relatedness on male reproductive success. RESULTS: We found that multiple paternity was very common (79% of broods), with up to five fathers contributing to a brood, though power was relatively low to detect more than four fathers. Density had a significant and positive linear effect on the number of fathers siring a brood, though this relationship leveled off at high numbers of fathers, which may reflect a lack of power and/or an upper limit to polyandry in this species. Significant skew in male reproductive contribution in multiply-sired broods was observed and we found a positive and significant relationship between the proportion of offspring sired and the genetic similarity between mates, suggesting that genetic compatibility may influence reproductive success in this species. CONCLUSIONS: To our knowledge, this is the first study to show high levels of multiple paternity in a barnacle, and overall, patterns of paternity in P. elegans appear to be driven primarily by mate availability. Evidence of paternity bias for males with higher relatedness suggests some form of post-copulatory sexual selection is taking place, but more work is needed to determine whether it operates during or post-fertilization. Overall, our results suggest that while polyandry in P. elegans is driven by mate availability, it may also provide a mechanism for females to ensure fertilization by compatible gametes and increase reproductive success in this sessile species.
Project description:Although the majority of passerine birds are socially monogamous, true genetic monogamy is rare, with extra-pair paternity (EPP) occurring in almost 90% of surveyed socially monogamous species. We present the first molecular data on the genetic breeding system of the long-tailed finch, Poephila acuticauda, a grass finch endemic to the tropical northern savannah of Australia. Although the species forms socially monogamous pair bonds during the breeding season, we found that extra-pair males sired 12.8% of 391 offspring, in 25.7% of 101 broods. Our findings provide only the second estimate of extra-pair paternity in the estrildid finch family.