A. Bradley Duthie

Quantifying inbreeding avoidance through extra-pair reproduction

Extra‐pair reproduction is widely hypothesized to allow females to avoid inbreeding with related socially paired males. Consequently, numerous field studies have tested the key predictions that extra‐pair offspring are less inbred than females’ alternative within‐pair offspring, and that the probability of extra‐pair reproduction increases with a females relatedness to her socially paired male. However, such studies rarely measure inbreeding or relatedness sufficiently precisely to detect subtle effects, or consider biases stemming from failure to observe inbred offspring that die during early development. Analyses of multigenerational song sparrow (Melospiza melodia) pedigree data showed that most females had opportunity to increase or decrease the coefficient of inbreeding of their offspring through extra‐pair reproduction with neighboring males. In practice, observed extra‐pair offspring had lower inbreeding coefficients than females’ within‐pair offspring on average, while the probability of extra‐pair reproduction increased substantially with the coefficient of kinship between a female and her socially paired male. However, simulations showed that such effects could simply reflect bias stemming from inbreeding depression in early offspring survival. The null hypothesis that extra‐pair reproduction is random with respect to kinship therefore cannot be definitively rejected in song sparrows, and existing general evidence that females avoid inbreeding through extra‐pair reproduction requires reevaluation given such biases.

When does female multiple mating evolve to adjust inbreeding?: Effects of inbreeding depression, direct costs, mating constraints, and polyandry as a threshold trait

Polyandry is often hypothesized to evolve to allow females to adjust the degree to which they inbreed. Multiple factors might affect such evolution, including inbreeding depression, direct costs, constraints on male availability, and the nature of polyandry as a threshold trait. Complex models are required to evaluate when evolution of polyandry to adjust inbreeding is predicted to arise. We used a genetically explicit individual‐based model to track the joint evolution of inbreeding strategy and polyandry defined as a polygenic threshold trait. Evolution of polyandry to avoid inbreeding only occurred given strong inbreeding depression, low direct costs, and severe restrictions on initial versus additional male availability. Evolution of polyandry to prefer inbreeding only occurred given zero inbreeding depression and direct costs, and given similarly severe restrictions on male availability. However, due to its threshold nature, phenotypic polyandry was frequently expressed even when strongly selected against and hence maladaptive. Further, the degree to which females adjusted inbreeding through polyandry was typically very small, and often reflected constraints on male availability rather than adaptive reproductive strategy. Evolution of polyandry solely to adjust inbreeding might consequently be highly restricted in nature, and such evolution cannot necessarily be directly inferred from observed magnitudes of inbreeding adjustment.

Trade-Offs and Coexistence in Fluctuating Environments: Evidence for a Key Dispersal-Fecundity Trade-Off in Five Nonpollinating Fig Wasps

The ecological principle of competitive exclusion states that species competing for identical resources cannot coexist, but this principle is paradoxical because ecologically similar competitors are regularly observed. Coexistence is possible under some conditions if a fluctuating environment changes the competitive dominance of species. This change in competitive dominance implies the existence of trade-offs underlying species’ competitive abilities in different environments. Theory shows that fluctuating distance between resource patches can facilitate coexistence in ephemeral patch competitors, given a functional trade-off between species dispersal ability and fecundity. We find evidence supporting this trade-off in a guild of five ecologically similar nonpollinating fig wasps and subsequently predict local among-patch species densities. We also introduce a novel colonization index to estimate relative dispersal ability among ephemeral patch competitors. We suggest that a dispersal ability–fecundity trade-off and spatiotemporally fluctuating resource availability commonly co-occur to drive population dynamics and facilitate coexistence in ephemeral patch communities.

What Happens after Inbreeding Avoidance? Inbreeding by Rejected Relatives and the Inclusive Fitness Benefit of Inbreeding Avoidance

Avoiding inbreeding, and therefore avoiding inbreeding depression in offspring fitness, is widely assumed to be adaptive in systems with biparental reproduction. However, inbreeding can also confer an inclusive fitness benefit stemming from increased relatedness between parents and inbred offspring. Whether or not inbreeding or avoiding inbreeding is adaptive therefore depends on a balance between inbreeding depression and increased parent-offspring relatedness. Existing models of biparental inbreeding predict threshold values of inbreeding depression above which males and females should avoid inbreeding, and predict sexual conflict over inbreeding because these thresholds diverge. However, these models implicitly assume that if a focal individual avoids inbreeding, then both it and its rejected relative will subsequently outbreed. We show that relaxing this assumption of reciprocal outbreeding, and the assumption that focal individuals are themselves outbred, can substantially alter the predicted thresholds for inbreeding avoidance for focal males. Specifically, the magnitude of inbreeding depression below which inbreeding increases a focal male’s inclusive fitness increases with increasing depression in the offspring of a focal female and her alternative mate, and it decreases with increasing relatedness between a focal male and a focal female’s alternative mate, thereby altering the predicted zone of sexual conflict. Furthermore, a focal male’s inclusive fitness gain from avoiding inbreeding is reduced by indirect opportunity costs if his rejected relative breeds with another relative of his. By demonstrating that variation in relatedness and inbreeding can affect intra- and inter-sexual conflict over inbreeding, our models lead to novel predictions for family dynamics. Specifically, parent-offspring conflict over inbreeding might depend on the alternative mates of rejected relatives, and male-male competition over inbreeding might lead to mixed inbreeding strategies. Making testable quantitative predictions regarding inbreeding strategies occurring in nature will therefore require new models that explicitly capture variation in relatedness and inbreeding among interacting population members.

Evolution of Inbreeding Avoidance and Inbreeding Preference through Mate Choice among Interacting Relatives

While extensive population genetic theory predicts conditions favoring evolution of self-fertilization versus outcrossing, there is no analogous theory that predicts conditions favoring evolution of inbreeding avoidance or inbreeding preference enacted through mate choice given obligate biparental reproduction. Multiple interacting processes complicate the dynamics of alleles underlying such inbreeding strategies, including sexual conflict, distributions of kinship, genetic drift, purging of mutation load, direct costs, and restricted kin discrimination. We incorporated these processes into an individual-based model to predict conditions where selection should increase or decrease frequencies of alleles causing inbreeding avoidance or inbreeding preference when females or males controlled mating. Selection for inbreeding avoidance occurred given strong inbreeding depression when either sex chose mates, while selection for inbreeding preference occurred given very weak inbreeding depression when females chose but never occurred when males chose. Selection for both strategies was constrained by direct costs and restricted kin discrimination. Purging was negligible, but allele frequencies were strongly affected by drift in small populations, while selection for inbreeding avoidance was weak in larger populations because inbreeding risk decreased. Therefore, while selection sometimes favored alleles underlying inbreeding avoidance or preference, evolution of such strategies may be much more restricted and stochastic than is commonly presumed.

Inbreeding parents should invest more resources in fewer offspring

Inbreeding increases parent–offspring relatedness and commonly reduces offspring viability, shaping selection on reproductive interactions involving relatives and associated parental investment (PI). Nevertheless, theories predicting selection for inbreeding versus inbreeding avoidance and selection for optimal PI have only been considered separately, precluding prediction of optimal PI and associated reproductive strategy given inbreeding. We unify inbreeding and PI theory, demonstrating that optimal PI increases when a females inbreeding decreases the viability of her offspring. Inbreeding females should therefore produce fewer offspring due to the fundamental trade-off between offspring number and PI. Accordingly, selection for inbreeding versus inbreeding avoidance changes when females can adjust PI with the degree that they inbreed. By contrast, optimal PI does not depend on whether a focal female is herself inbred. However, inbreeding causes optimal PI to increase given strict monogamy and associated biparental investment compared with female-only investment. Our model implies that understanding evolutionary dynamics of inbreeding strategy, inbreeding depression, and PI requires joint consideration of the expression of each in relation to the other. Overall, we demonstrate that existing PI and inbreeding theories represent special cases of a more general theory, implying that intrinsic links between inbreeding and PI affect evolution of behaviour and intrafamilial conflict.

Demographic mechanisms of inbreeding adjustment through extra-pair reproduction.

One hypothesis explaining extra-pair reproduction is that socially monogamous females mate with extra-pair males to adjust the coefficient of inbreeding (f) of extra-pair offspring (EPO) relative to that of within-pair offspring (WPO) they would produce with their socially paired male. Such adjustment of offspring f requires non-random extra-pair reproduction with respect to relatedness, which is in turn often assumed to require some mechanism of explicit pre-copulatory or post-copulatory kin discrimination. We propose three demographic processes that could potentially cause mean f to differ between individual females’ EPO and WPO given random extra-pair reproduction with available males without necessarily requiring explicit kin discrimination. Specifically, such a difference could arise if social pairings formed non-randomly with respect to relatedness or persisted non-randomly with respect to relatedness, or if the distribution of relatedness between females and their sets of potential mates changed during the period through which social pairings persisted. We used comprehensive pedigree and pairing data from free-living song sparrows (Melospiza melodia) to quantify these three processes and hence investigate how individual females could adjust mean offspring f through instantaneously random extra-pair reproduction. Female song sparrows tended to form social pairings with unrelated or distantly related males slightly less frequently than expected given random pairing within the defined set of available males. Furthermore, social pairings between more closely related mates tended to be more likely to persist across years than social pairings between less closely related mates. However, these effects were small and the mean relatedness between females and their sets of potential extra-pair males did not change substantially across the years through which social pairings persisted. Our framework and analyses illustrate how demographic and social structuring within populations might allow females to adjust mean f of offspring through random extra-pair reproduction without necessarily requiring explicit kin discrimination, implying that adjustment of offspring f might be an inevitable consequence of extra-pair reproduction. New theoretical and empirical studies are required to explore the general magnitude of such effects and quantify the degree to which they could facilitate or constrain long-term evolution of extra-pair reproduction.

Resolving the conundrum of inbreeding depression but no inbreeding avoidance: Estimating sex‐specific selection on inbreeding by song sparrows (Melospiza melodia)

Inbreeding avoidance among interacting females and males is not always observed despite inbreeding depression in offspring fitness, creating an apparent “inbreeding paradox.” This paradox could be resolved if selection against inbreeding was in fact weak, despite inbreeding depression. However, the net magnitude and direction of selection on the degree to which females and males inbreed by pairing with relatives has not been explicitly estimated. We used long‐term pedigree data to estimate phenotypic selection gradients on the degree of inbreeding that female and male song sparrows (Melospiza melodia) expressed by forming socially persistent breeding pairs with relatives. Fitness was measured as the total numbers of offspring and grand offspring contributed to the population, and as corresponding expected numbers of identical‐by‐descent allele copies, thereby accounting for variation in offspring survival, reproduction, and relatedness associated with variation in parental inbreeding. Estimated selection gradients on the degree to which individuals paired with relatives were weakly positive in females, but negative in males that formed at least one socially persistent pairing. However, males that paired had higher mean fitness than males that remained socially unpaired. These analyses suggest that net selection against inbreeding may be weak in both sexes despite strong inbreeding depression, thereby resolving the “inbreeding paradox.”

Trade-Offs and Coexistence: A Lottery Model Applied to Fig Wasp Communities

Ecological communities in which organisms complete their life cycles on discrete ephemeral patches are common and often support an unusually large number of species. Explaining this diversity is challenging for communities of ecologically similar species undergoing preemptive competition, where classic coexistence mechanisms may not readily apply. We use nonpollinating fig wasps as a model community characterized by high diversity and preemptive competition to show how subadditive population growth and a trade-off between competitor fecundity and dispersal ability can lead to coexistence. Because nonpollinator species are often closely related, have similar life histories, and compete for the same discrete resources, understanding their coexistence is challenging given competitive exclusion is expected. Empirical observations suggest that nonpollinating fig wasp species may face a trade-off between egg loads and dispersal abilities. We model a lottery in which a species’ competitive ability is determined by a trade-off between fecundity and dispersal ability. Variation in interpatch distance between figs generates temporal variability in the relative benefit of fecundity versus dispersal. We show that the temporal storage effect leads to coexistence for a range of biologically realistic parameter values. We further use individual-based modeling to show that when species’ traits evolve, coexistence is less likely but trait divergence can result. We discuss the implications of this coexistence mechanism for ephemeral patch systems wherein competition is strongly preemptive.

Evolution of precopulatory and post-copulatory strategies of inbreeding avoidance and associated polyandry

Inbreeding depression is widely hypothesized to drive adaptive evolution of precopulatory and post‐copulatory mechanisms of inbreeding avoidance, which in turn are hypothesized to affect evolution of polyandry (i.e. female multiple mating). However, surprisingly little theory or modelling critically examines selection for precopulatory or post‐copulatory inbreeding avoidance, or both strategies, given evolutionary constraints and direct costs, or examines how evolution of inbreeding avoidance strategies might feed back to affect evolution of polyandry. Selection for post‐copulatory inbreeding avoidance, but not for precopulatory inbreeding avoidance, requires polyandry, whereas interactions between precopulatory and post‐copulatory inbreeding avoidance might cause functional redundancy (i.e. ‘degeneracy’) potentially generating complex evolutionary dynamics among inbreeding strategies and polyandry. We used individual‐based modelling to quantify evolution of interacting precopulatory and post‐copulatory inbreeding avoidance and associated polyandry given strong inbreeding depression and different evolutionary constraints and direct costs. We found that evolution of post‐copulatory inbreeding avoidance increased selection for initially rare polyandry and that evolution of a costly inbreeding avoidance strategy became negligible over time given a lower‐cost alternative strategy. Further, fixed precopulatory inbreeding avoidance often completely precluded evolution of polyandry and hence post‐copulatory inbreeding avoidance, but fixed post‐copulatory inbreeding avoidance did not preclude evolution of precopulatory inbreeding avoidance. Evolution of inbreeding avoidance phenotypes and associated polyandry is therefore affected by evolutionary feedbacks and degeneracy. All else being equal, evolution of precopulatory inbreeding avoidance and resulting low polyandry is more likely when post‐copulatory inbreeding avoidance is precluded or costly, and evolution of post‐copulatory inbreeding avoidance greatly facilitates evolution of costly polyandry.