Fecundity, offspring longevity, and assortative mating: parametric tradeoffs in sexual and life history strategy

Genetic diversification of offspring represents a bet-hedging strategy that evolved as an adaptation to unpredictable environments. The benefits of sexual reproduction come with severe costs. For example, each offspring only carries half of each parent's genetic makeup through direct descent. The lower the reproductive rate, the more substantial the cost when considering the proportion of genes represented in subsequent generations. Positive assortative mating represents a conservative bet-hedging strategy that offsets some of these costs and preserves coadapted genomes in stable and predictable environments, whereas negative assortative mating serves the inverse function of genetic diversification in unstable and unpredictable environments.     

Female multiple mating as a genetic bet-hedging strategy when mate choice criteria are unreliable

Female multiple mating (or polyandry) is considered to act as a genetic bet-hedging mechanism, by which females can reduce the assessment error in regard to mates genetic quality when only uncertain information is available. In spite of frequent verbal arguments, no theoretical examination has been carried out to determine the effectiveness of bet-hedging by multiple mating. In the present paper, I show that three factors, female population size, remating costs and environmental fluctuation, all affect the effectiveness of bet-hedging. A mathematical model predicts that bet-hedging effectively works only in small populations, and computer simulations were used to confirm this prediction. The results of simulations differed according to the degree of environmental fluctuation. In relatively stable environments, if there is no remating cost, the fixation probability of a multiple mating strategy is slightly higher than that of a single mating strategy, independent of female population size. However, with very slight fitness costs, multiple mating drastically loses its advantage as population size increases, and almost always becomes extinct within large populations. This means that the evolution of polyandry solely by the mechanism of bet-hedging is unlikely in stable environments. However, in unpredictable environments, or when negative frequency-dependent selection on fitness-related loci is introduced, a multiple mating strategy is sometimes successful against a single mating strategy, even if it entails a small fitness cost. Therefore, female multiple mating may possibly evolve only in these limited conditions. In most cases, some deterministic mechanisms such as postcopulatory sperm selection by multiply mated females (or direct material benefits) are more reasonable as the evolutionary causes of polyandry.     

Assortative Pairing and Life History Strategy

A secondary analysis was performed on preliminary data from an ongoing cross-cultural study on assortative pairing. Independently sampled pairs of opposite-sex romantic partners and of same-sex friends rated themselves and each other on Life History (LH) strategy and mate value. Data were collected in local bars, clubs, coffeehouses, and other public places from three different cultures: Tucson, Arizona; Hermosillo, Sonora; and San José, Costa Rica. The present analysis found that slow LH individuals assortatively pair with both sexual and social partners more strongly than fast LH individuals. We interpret this phenomenon as representing (1) an adaptation for preserving coadapted genomes in slow LH strategists to maintain high copying fidelity genetic replication while producing a lower number of offspring in stable, predictable, and controllable environments and (2) a bet-hedging adaptation in fast LH strategists, favoring the genetic diversification of a higher number of offspring in unstable, unpredictable, and uncontrollable environments.

Spatial variation in egg size and egg number reflects trade-offs and bet-hedging in a freshwater fish

1.?Maternal reproductive investment is thought to reflect a trade-off between offspring size and fecundity, and models generally predict that mothers inhabiting adverse environments will produce fewer, larger offspring. More recently, the importance of environmental unpredictability in influencing maternal investment has been considered, with some models predicting that mothers should adopt a diversified bet-hedging strategy whilst others a conservative bet-hedging strategy. 2.?We explore spatial egg size and fecundity patterns in the freshwater fish southern pygmy perch (Nannoperca australis) that inhabits a diversity of streams along gradients of environmental quality, variability and predictability. 3.?Contrary to some predictions, N.?australis populations inhabiting increasingly harsh streams produced more numerous and smaller eggs. Furthermore, within-female egg size variability increased as environments became more unpredictable. 4.?We argue that in harsh environments or those prone to physical disturbance, sources of mortality are size independent with offspring size having only a minor influence on offspring fitness. Instead, maternal fitness is maximized by producing many small eggs, increasing the likelihood that some offspring will disperse to permanent water. We also provide empirical support for diversified bet-hedging as an adaptive strategy when future environmental quality is uncertain and suggest egg size may be a more appropriate fitness measure in stable environments characterized by size-dependent fitness. These results likely reflect spatial patterns of adaptive plasticity and bet-hedging in response to both predictable and unpredictable environmental variance and highlight the importance of considering both trait averages and variance. 5.?Reproductive life-history traits can vary predictably along environmental gradients. Human activity, such as the hydrological modification of natural flow regimes, alters the form and magnitude of these gradients, and this can have both ecological and evolutionary implications for biota adapted to now non-existent natural environmental heterogeneity.     

High Altitude Frogs (Rana kukonoris) Adopt a Diversified Bethedging Strategy in the Face of Environmental Unpredictability

Environmental unpredictability can influence strategies of maternal investment among eggs within a clutch. Models predict that breeding females should adopt a diversified bet-hedging strategy in unpredictable environments, but empirical field evidence from Asia is scarce. Here we tested this hypothesis by exploring spatial patterns in egg size along an altitudinal gradient in a frog species(Rana kukunoris) inhabiting the Tibetan Plateau. Within-clutch variability in egg size increased as the environment became variable(e.g., lower mean monthly temperature and mean monthly rainfall at higher altitudes), and populations in environments with more unpredictable rainfall produced eggs that were smaller and more variable in size. We provide support for a diversified bet-hedging strategy in high-altitude environments, which experience dynamic weather patterns and therefore are of unpredictable environmental quality. This strategy may be an adaptive response to lower environmental quality and higher unpredictable environmental variance. Such a strategy should increase the likelihood of breeding success and maximize maternal lifetime fitness by producing offspring that are adapted to current environmental conditions. We speculate that in high-altitude environments prone to physical disturbance, breeding females are unable to consistently produce the optimal egg size due to physiological constraints imposed by environmental conditions(e.g., duration of the active season, food availability). Species and populations whose breeding strategies are adapted to cope with uncertain environmental conditions by adjusting offspring size and therefore quality show a remarkable degree of ability to cope with future climatic changes.     

Testing the role of coadapted genes versus bet-hedging for mating strategies in colour polymorphic pygmy grasshoppers

Recent investigations of mate choice indicate that the genetic effect of sires on offspring fitness may depend on the interaction between maternal and paternal genotypes and the environmental conditions experienced by the offspring. Alternative colour morphs of the pygmy grasshopper, Tetrix subulata , represent ecological strategies that differ in body size, life history, thermoregulatory behaviour, and habitat selection. The hypothesis that selection promotes behaviours maintaining coadapted gene complexes predicts individuals to mate assortatively with respect to colour morph. On the other hand, the bet-hedging hypothesis predicts that the temporal variability of the environment inhabited by these animals may select for disassortative mating behaviour resulting in heterogeneous offspring. To distinguish between these competing hypotheses, we investigated mating behaviours using dual-choice experiments. Our results were not in agreement with the prediction of assortative mating but suggest instead that matings were random with regard to colour morph. Polyandry was common, and females mated with the second male regardless of whether the first mating was assortative or disassortative. Polyandry also was equally frequent among females in triads in which the two males belonged to different colour morphs as in triads where both males belonged to the same colour morph. A field experiment confirmed that polyandry occurred also among free-ranging individuals, and uncovered variation in mating success among male colour morphs, probably due to indirect effects of coloration on activity or habitat use. The consequences of this random and polyandrous mating strategy for the evolutionary dynamics of the colour polymorphism remain to be explored.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 491–499.     

Mate choice for major histocompatibility complex genetic divergence as a bet-hedging strategy in the Atlantic salmon (Salmo salar)

Major histocompatibility complex (MHC)-dependent mating preferences have been observed across vertebrate taxa and these preferences are expected to promote offspring disease resistance and ultimately, viability. However, little empirical evidence linking MHC-dependent mate choice and fitness is available, particularly in wild populations. Here, we explore the adaptive potential of previously observed patterns of MHC-dependent mate choice in a wild population of Atlantic salmon (Salmo salar) in Québec, Canada, by examining the relationship between MHC genetic variation and adult reproductive success and offspring survival over 3 years of study. While Atlantic salmon choose their mates in order to increase MHC diversity in offspring, adult reproductive success was in fact maximized between pairs exhibiting an intermediate level of MHC dissimilarity. Moreover, patterns of offspring survival between years 0+ and 1+, and 1+ and 2+ and population genetic structure at the MHC locus relative to microsatellite loci indicate that strong temporal variation in selection is likely to be operating on the MHC. We interpret MHC-dependent mate choice for diversity as a likely bet-hedging strategy that maximizes parental fitness in the face of temporally variable and unpredictable natural selection pressures.     

Bet-hedging as an evolutionary game: the trade-off between egg size and number

Bet-hedging theory addresses how individuals should optimize fitness in varying and unpredictable environments by sacrificing mean fitness to decrease variation in fitness. So far, three main bet-hedging strategies have been described: conservative bet-hedging (play it safe), diversified bet-hedging (don’t put all eggs in one basket) and adaptive coin flipping (choose a strategy at random from a fixed distribution). Within this context, we analyse the trade-off between many small eggs (or seeds) and few large, given an unpredictable environment. Our model is an extension of previous models and allows for any combination of the bet-hedging strategies mentioned above. In our individual-based model (accounting for both ecological and evolutionary forces), the optimal bet-hedging strategy is a combination of conservative and diversified bet-hedging and adaptive coin flipping, which means a variation in egg size both within clutches and between years. Hence, we show how phenotypic variation within a population, often assumed to be due to non-adaptive variation, instead can be the result of females having this mixed strategy. Our results provide a new perspective on bet-hedging and stress the importance of extreme events in life history evolution.     

Assortative mating and offspring well-being: theory and empirical findings from a native Amazonian society in Bolivia

Mate choice matters for inclusive fitness, household economic efficiency, assimilation, stratification, and economic inequalities in society. In positive assortative mating, people pair with someone who resembles them along a trait, whereas in negative assortative mating, people pair with someone who differs from them along a trait. In industrial nations, people tend to follow positive assortative mating for fundamental demographic dimensions (e.g., age, schooling) and might practice negative assortative mating for economic outcomes (e.g., earnings). Research on assortative mating has focused on industrial nations, generally compared only one trait between couples, and paid scant attention to the effects of assortative mating for offspring well-being. If assortative mating enhances inclusive fitness, it might also enhance offspring well-being. Drawing on data from a farming–foraging society in the Bolivian Amazon (Tsimane') that practices preferential cross-cousin marriage, we (a) identify six parental traits (age, knowledge, wealth, schooling, height, and smiles) for which Tsimane' might practice assortative mating and (b) test the hypothesis that assortative mating enhances offspring well-being. Proxies for offspring well-being include height and school attainment. Tsimane' resemble people of industrial nations in practicing mostly positive assortative mating. Pairwise, mother–father and Pearson correlations of age, schooling, and earnings among Tsimane' resemble correlations of industrial nations. Correlation coefficients for the six parental traits were far higher than correlations that might happened just by chance. We found weak support for the hypothesis that assortative mating improves offspring well-being.     

Genetic and morphological divergence along the littoral–pelagic axis in two common and sympatric fishes: perch,Perca fluviatilis (Percidae) and roach,Rutilus rutilus (Cyprinidae)

Individuals are constantly in competition with one another and, on both ecological and evolutionary timescales, processes act to reduce this competition and promote the gain of fitness advantages via diversification. Here we have investigated the genetic (AFLP) and morphological (geometric morphometrics) aspects of the littoral–pelagic axis, a commonly observed resource polymorphism in freshwater fishes of postglacial lakes. We found a large degree of variation in the genetic and morphological divergence between littoral and pelagic perch and roach across Swedish lakes. Although there was evidence of assortative mating (elevated kinship values) in both species, we could not find any significant coupling of morphology and genetic divergence. Instead, there was evidence that the extent of resource polymorphism may be largely caused by phenotypic plasticity. These results suggest that assortative mating, which can lead to genetically determined adaptive divergence, does occur in these species, particularly perch, but not according to genetically fixed morphological traits. The behavioural mechanisms facilitating associative mating need to be investigated to explore the interaction between phenotypic plasticity and adaptive genetic divergence and their roles in diversification. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 929–940.     

Direct fitness benefits explain mate preference,but not choice,for similarity in heterozygosity levels

Under sexual selection, mate preferences can evolve for traits advertising fitness benefits. Observed mating patterns (mate choice) are often assumed to represent preference, even though they result from the interaction between preference, sampling strategy and environmental factors. Correlating fitness with mate choice instead of preference will therefore lead to confounded conclusions about the role of preference in sexual selection. Here we show that direct fitness benefits underlie mate preferences for genetic characteristics in a unique experiment on wild great tits. In repeated mate preference tests, both sexes preferred mates that had similar heterozygosity levels to themselves, and not those with which they would optimise offspring heterozygosity. In a subsequent field experiment where we cross fostered offspring, foster parents with more similar heterozygosity levels had higher reproductive success, despite the absence of assortative mating patterns. These results support the idea that selection for preference persists despite constraints on mate choice.     

Mate choice evolution, dominance effects, and the maintenance of genetic variation

Female mate choice influences the maintenance of genetic variation by altering the mating success of males with different genotypes. The evolution of preferences themselves, on the other hand, depends on genetic variation present in the population. Few models have tracked this feedback between a choice gene and its effects on genetic variation, in particular when genes that determine offspring viability and attractiveness have dominance effects. Here we build a population genetic model that allows comparing the evolution of various choice rules in a single framework. We first consider preferences for good genes and show that focused preferences for homozygotes evolve more easily than broad preferences, which allow heterozygous males high mating success too. This occurs despite better maintenance of genetic diversity in the latter scenario, and we discuss why empirical findings of superior mating success of heterozygous males consequently do not immediately lead to a better understanding of the lek paradox. Our results thus suggest that the mechanisms that help maintain genetic diversity also have a flipside of making female choice an inaccurate means of producing the desired kind of offspring. We then consider preferences for heterozygosity per se, and show that these evolve only under very special conditions. Choice for compatible genotypes can evolve but its selective advantage diminishes quickly due to frequency-dependent selection. Finally, we show that our model reproduces earlier results on selfing, when the female choice strategy produces assortative mating. Overall, our model indicates that various forms of heterozygote-favouring (or variable) female choice pose a problem for the theory of sexual ornamentation based on indirect benefits, rather than a solution.     

Limits to the evolution of assortative mating by female choice under restricted gene flow

The evolution of assortative mating is a key component of the process of speciation with gene flow. Several recent theoretical studies have pointed out, however, that sexual selection which can result from assortative mating may cause it to plateau at an intermediate level; this is primarily owing to search costs of individuals with extreme phenotypes and to assortative preferences developed by individuals with intermediate phenotypes. I explore the limitations of assortative mating further by analysing a simple model in which these factors have been removed. Specifically, I use a haploid two-population model to ask whether the existence of assortative mating is sufficient to drive the further evolution of assortative mating. I find that a weakening in the effective strength of sexual selection with strong assortment leads to the existence of both a peak level of trait differentiation and the evolution of an intermediate level of assortative mating that will cause that peak. This result is robust to the inclusion of local adaptation and different genetic architecture of the trait. The results imply the existence of fundamental limits to the evolution of assortment via sexual selection in this situation, with which other factors, such as search costs, may interact.     

Why do females mate multiply? A review of the genetic benefits

The aim of this review is to consider the potential benefits that females may gain from mating more than once in a single reproductive cycle. The relationship between non-genetic and genetic benefits is briefly explored. We suggest that multiple mating for purely non-genetic benefits is unlikely as it invariably leads to the possibility of genetic benefits as well. We begin by briefly reviewing the main models for genetic benefits to mate choice, and the supporting evidence that choice can increase offspring performance and the sexual attractiveness of sons. We then explain how multiple mating can elevate offspring fitness by increasing the number of potential sires that compete, when this occurs in conjunction with mechanisms of paternity biasing that function in copula or post-copulation. We begin by identifying cases where females use pre-copulatory cues to identify mates prior to remating. In the simplest case, females remate because they identify a superior mate and 'trade up' genetically. The main evidence for this process comes from extra-pair copulation in birds. Second, we note other cases where pre-copulatory cues may be less reliable and females mate with several males to promote post-copulatory mechanisms that bias paternity. Although a distinction is drawn between sperm competition and cryptic female choice, we point out that the genetic benefits to polyandry in terms of producing more viable or sexually attractive offspring do not depend on the exact mechanism that leads to biased paternity. Post-copulatory mechanisms of paternity biasing may: (1) reduce genetic incompatibility between male and female genetic contributions to offspring; (2) increase offspring viability if there is a positive correlation between traits favoured post-copulation and those that improve performance under natural selection; (3) increase the ability of sons to gain paternity when they mate with polyandrous females. A third possibility is that genetic diversity among offspring is directly favoured. This can be due to bet-hedging (due to mate assessment errors or temporal fluctuations in the environment), beneficial interactions between less related siblings or the opportunity to preferentially fertilise eggs with sperm of a specific genotype drawn from a range of stored sperm depending on prevailing environmental conditions. We use case studies from the social insects to provide some concrete examples of the role of genetic diversity among progeny in elevating fitness. We conclude that post-copulatory mechanisms provide a more reliable way of selecting a genetically compatible mate than pre-copulatory mate choice. Some of the best evidence for cryptic female choice by sperm selection is due to selection of more compatible sperm. Two future areas of research seem likely to be profitable. First, more experimental evidence is needed demonstrating that multiple mating increases offspring fitness via genetic gains. Second, the role of multiple mating in promoting assortative fertilization and increasing reproductive isolation between populations may help us to understand sympatric speciation.     

Sexual dimorphism and adaptive speciation: two sides of the same ecological coin

Models of adaptive speciation are typically concerned with demonstrating that it is possible for ecologically driven disruptive selection to lead to the evolution of assortative mating and hence speciation. However, disruptive selection could also lead to other forms of evolutionary diversification, including ecological sexual dimorphisms. Using a model of frequency-dependent intraspecific competition, we show analytically that adaptive speciation and dimorphism require identical ecological conditions. Numerical simulations of individual-based models show that a single ecological model can produce either evolutionary outcome, depending on the genetic independence of male and female traits and the potential strength of assortative mating. Speciation is inhibited when the genetic basis of male and female ecological traits allows the sexes to diverge substantially. This is because sexual dimorphism, which can evolve quickly, can eliminate the frequency-dependent disruptive selection that would have provided the impetus for speciation. Conversely, populations with strong assortative mating based on ecological traits are less likely to evolve a sexual dimorphism because females cannot simultaneously prefer males more similar to themselves while still allowing the males to diverge. This conflict between speciation and dimorphism can be circumvented in two ways. First, we find a novel form of speciation via negative assortative mating, leading to two dimorphic daughter species. Second, if assortative mating is based on a neutral marker trait, trophic dimorphism and speciation by positive assortative mating can occur simultaneously. We conclude that while adaptive speciation and ecological sexual dimorphism may occur simultaneously, allowing for sexual dimorphism restricts the likelihood of adaptive speciation. Thus, it is important to recognize that disruptive selection due to frequency-dependent interactions can lead to more than one form of adaptive splitting.     

Stress-induced assortative mating and the evolution of stress resistance

We show with a model that variation in environmental stress between generations facilitates the evolution of stress resistance through assortative mating. Stress induces delayed maturation of susceptible phenotypes, segregating their fertile period from resistant phenotypes. Assortment of mates enhances the responsiveness of populations to natural selection by inflating genetic variance. Thus, positive selection and inflated genetic variance in stressful environments can cause a strong evolutionary increase in resistance. By contrast, benign environments do not segregate phenotypes, and the random mating among phenotypes deflates genetic variance, leading to a weaker response to selection against resistance, assuming that resistance is costly. When environments vary randomly from benign to stressful, populations respond asymmetrically to negative and positive selection. This asymmetry (1) accelerates fixation of a resistance allele if resistance is generally favoured (stressful generations more frequent) but delays the loss of the allele if it is generally disfavoured (benign generations more frequent), and (2) it can push a resistance allele to fixation even when long‐term costs modestly exceed benefits. When resistance alleles pleiotropically delay mating, stress‐induced random mating has complementary effects. Serial autocorrelation in the stressor amplifies these effects. These results suggest a novel mechanism for the persistence of resistance polymorphisms.     

Asymmetric dominance and asymmetric mate choice oppose premating isolation after allopatric divergence

Assortative mating promotes reproductive isolation and allows allopatric speciation processes to continue in secondary contact. As mating patterns are determined by mate preferences and intrasexual competition, we investigated male–male competition and behavioral isolation in simulated secondary contact among allopatric populations. Three allopatric color morphs of the cichlid fish Tropheus were tested against each other. Dyadic male–male contests revealed dominance of red males over bluish and yellow‐blotch males. Reproductive isolation in the presence of male–male competition was assessed from genetic parentage in experimental ponds and was highly asymmetric among pairs of color morphs. Red females mated only with red males, whereas the other females performed variable degrees of heteromorphic mating. Discrepancies between mating patterns in ponds and female preferences in a competition‐free, two‐way choice paradigm suggested that the dominance of red males interfered with positive assortative mating of females of the subordinate morphs and provoked asymmetric hybridization. Between the nonred morphs, a significant excess of negative assortative mating by yellow‐blotch females with bluish males did not coincide with asymmetric dominance among males. Hence, both negative assortative mating preferences and interference of male–male competition with positive assortative preferences forestall premating isolation, the latter especially in environments unsupportive of competition‐driven spatial segregation.     

Disturbance induces the contrasting evolution of reinforcement and dispersiveness in directed and random movers

Spatial models commonly assume that dispersal rates are constant across individuals and environments and that movement directions are unbiased. These random-movement assumptions are inadequate to capture the range of dispersal behaviors revealed in diverse case studies. We examine an alternative assumption of directed movement, in which dispersal is a conditional and directional response by individuals to varying environmental conditions. Specifically, we assume individuals bias their movements to climb spatial fitness gradients. We compare the consequences of random and directed movement for local adaptation, the evolution of dispersal, and the reinforcement process. The implications of each movement strategy depend on the nature of environmental disturbance, and we examine the outcomes for undisturbed environments and with uncorrelated and autocorrelated disturbances. Both movement strategies offer advantages over sedentary life histories by allowing colonization of suitable habitats. However, random movement eventually becomes costly in stable environments because it inhibits local adaptation. In contrast, directed movement accelerates local adaptation. In disturbed environments, random movement offers bet-spreading advantages by distributing offspring across habitats. Despite being a more targeted strategy, an intermediate amount of directed movement provides similar bet-spreading benefits. These fitness consequences have implications for the evolution of dispersal. Dispersiveness is lost by random movers in undisturbed environments, is maintained in polymorphism with infrequent disturbances, and evolves when disturbances are uncorrelated. Directed movement becomes selectively neutral in the absence of disturbance, evolves when disturbances are autocorrelated, and is maintained in polymorphism with uncorrelated disturbances. Disturbance also determines the outcome of the reinforcement process for each strategy. For example, directed movers show no progress toward reinforcement in undisturbed environments, evolve random mating with uncorrelated disturbances, and can evolve assortative mating in infrequently disturbed environments.     

MULTIPLE MATING IN THE GLANVILLE FRITILLARY BUTTERFLY: A CASE OF WITHIN‐GENERATION BET HEDGING?

Many hypotheses have been proposed to explain multiple mating in females. One of them is bet hedging, that is avoiding having no or very few offspring in any given generation, rather than maximizing the expected number of offspring. However, within-generation bet hedging is generally believed to be an unimportant evolutionary force, except in very small populations. In this study, we derive predictions of the bet-hedging hypothesis for a case in which local insect populations are often small, offspring performance varies, for example, due to inbreeding depression, and the groups of gregarious larvae have to exceed a threshold size before they are likely to survive throughout the larval stage. These conditions exist for populations of the Glanville fritillary butterfly (Melitaea cinxia), potentially making bet-hedging benefits larger than usual. We observed matings in a field cage, which allowed detailed observations under practically natural conditions, and analyzed genetic paternity of egg clutches laid by females under direct observation. The egg-laying and survival patterns are in line with the predictions, supporting the hypothesis that multiple mating in M. cinxia presents a rare case of within-generation bet hedging.     

Ecological, social, and genetic contingency of extrapair behavior in a socially monogamous bird

Extrapair mating strategies are common among socially monogamous birds, but vary widely across ecological and social contexts in which breeding occurs. This variation is thought to reflect a compromise between the direct costs of mates' extrapair behavior and indirect benefits of extrapair fertilizations (EPF) to offspring fitness. However, in most free-living populations, the complete spatial and temporal distribution of mating attempts, genetic characteristics of available mates, and their relative contribution to EPF strategies are difficult to assess. Here we examined prevalence of EPF in relation to breeding density, synchrony, and genetic variability of available mates in a wild population of house finches Carpodacus mexicanus where all breeding attempts are known and all offspring are genotyped. We found that 15% of 59 nests contained extra-pair offspring and 9% of 212 offspring were sired by extra-pair males. We show experimentally that paired males and females avoided EPF displays in the presence of their social partners, revealing direct selection against EPF behavior. However, at the population level, the occurrence of EPF did not vary with nests dispersion, initiation date, synchrony, or with distance between the nests of extrapair partners. Instead, the occurrence of EPF closely covaried with genetic relatedness of a pool of available mates and offspring of genetically dissimilar mating tended to be resistant to a novel pathogen. These results corroborate findings that, in this population, strong fitness benefits of EPF are specific to each individual, thus highlighting the ecological, social, and genetic contingency of costs and benefits of an individual's extrapair behaviors.