The fitness consequences of wildlife conservation translocations: a meta-analysis.

Conservation translocation is a common strategy to offset mounting rates of population declines through the transfer of captive- or wild-origin organisms into areas where conspecific populations are imperilled or completely extirpated. Translocations that supplement existing populations are referred to as reinforcements and can be conducted using captive-origin animals [ex situ reinforcement (ESR)] or wild-origin animals without any captive ancestry [in situ reinforcement (ISR)]. These programs have been criticized for low success rates and husbandry practices that produce individuals with genetic and performance deficits, but the post-release performance of captive-origin or wild-origin translocated groups has not been systematically reviewed to quantify success relative to wild-resident control groups. To assess the disparity in post-release performance of translocated organisms relative to wild-resident conspecifics and examine the association of performance disparity with organismal and methodological factors across studies, we conducted a systematic review and meta-analysis of 821 performance comparisons from 171 studies representing nine animal classes (101 species). We found that translocated organisms have 64% decreased odds of out-performing their wild-resident counterparts, supporting claims of systemic issues hampering conservation translocations. To help identify translocation practices that could maximize program success in the future, we further quantified the impact of broad organismal and methodological factors on the disparity between translocated and wild-resident conspecific performance. Pre-release animal enrichment significantly reduced performance disparities, whereas our results suggest no overall effects of taxonomic group, sex, captive generation time, or the type of fitness surrogate measured. This work is the most comprehensive systematic review to date of animal conservation translocations in which wild conspecifics were used as comparators, thereby facilitating an evaluation of the overall impact of this conservation strategy and identifying specific actions to increase success. Our review highlights the need for conservation managers to include both sympatric and allopatric wild-reference groups to ensure the post-release performance of translocated animals can be evaluated. Further, our analyses identify pre-release animal enrichment as a particular strategy for improving the outcomes of animal conservation translocations, and demonstrate how meta-analysis can be used to identify implementation choices that maximize translocated animal contributions to recipient population growth and viability.

Tests for associations between sexual dimorphism and patterns of quantitative genetic variation in the water strider, Aquarius remigis.

The evolution of sexual dimorphisms requires divergence between sexes in the evolutionary trajectories of the traits involved. Discerning how genetic architecture could facilitate such divergence has proven challenging because of the difficulty in estimating non-additive and sex-linked genetic variances using traditional quantitative genetic designs. Here we use a three-generation, double-first-cousin pedigree design to estimate additive, sex-linked and dominance (co)variances for 12 traits in the water strider, Aquarius remigis. Comparisons among these traits, which have size ratios ranging from 1 to 5 (larger/smaller), allow us to ask if sexual dimorphisms are associated with characteristic patterns of quantitative genetic variation. We frame our analysis around three main questions, derived from existing theory and empirical evidence: Are sexual dimorphisms associated with (1) lower additive inter-sex genetic correlations, (2) higher proportions of sex-linked variance, or (3) differences between sexes in autosomal additive and dominance genetic variances? For questions (1) and (2), we find weak and non-significant trends in the expected directions, which preclude definitive conclusions. However, in answer to question (3), we find strong evidence for a positive relationship between sexual dimorphism and differences between sexes in proportions of autosomal dominance variance. We also find strong interactions among the three genetic components indicating that their relative influence differs among traits and between sexes. These results highlight the need to include all three components of genetic (co)variance in both theoretical evolutionary models and empirical estimations of the genetic architecture of dimorphic traits.

Genetic variation underlies plastic responses to global change drivers in the purple sea urchin, Strongylocentrotus purpuratus.

Phenotypic plasticity and adaptive evolution enable population persistence in response to global change. However, there are few experiments that test how these processes interact within and across generations, especially in marine species with broad distributions experiencing spatially and temporally variable temperature and pCO2. We employed a quantitative genetics experiment with the purple sea urchin, Strongylocentrotus purpuratus, to decompose family-level variation in transgenerational and developmental plastic responses to ecologically relevant temperature and pCO2. Adults were conditioned to controlled non-upwelling (high temperature, low pCO2) or upwelling (low temperature, high pCO2) conditions. Embryos were reared in either the same conditions as their parents or the crossed environment, and morphological aspects of larval body size were quantified. We find evidence of family-level phenotypic plasticity in response to different developmental environments. Among developmental environments, there was substantial additive genetic variance for one body size metric when larvae developed under upwelling conditions, although this differed based on parental environment. Furthermore, cross-environment correlations indicate significant variance for genotype-by-environment interactive effects. Therefore, genetic variation for plasticity is evident in early stages of S. purpuratus, emphasizing the importance of adaptive evolution and phenotypic plasticity in organismal responses to global change.

Reduced Mitochondrial Respiration in Hybrid Asexual Lizards.

AbstractThe scarcity of asexual reproduction in vertebrates alludes to an inherent cost. Several groups of asexual vertebrates exhibit lower endurance capacity (a trait predominantly sourced by mitochondrial respiration) compared with congeneric sexual species. Here we measure endurance capacity in five species of Aspidoscelis lizards and examine mitochondrial respiration between sexual and asexual species using mitochondrial respirometry. Our results show reduced endurance capacity, reduced mitochondrial respiration, and reduced phenotypic variability in asexual species compared with parental sexual species, along with a positive relationship between endurance capacity and mitochondrial respiration. Results of lower endurance capacity and lower mitochondrial respiration in asexual Aspidoscelis are consistent with hypotheses involving mitonuclear incompatibility.

Rapid evolution of sexual size dimorphism facilitated by Y-linked genetic variance.

Sexual dimorphism is ubiquitous in nature but its evolution is puzzling given that the mostly shared genome constrains independent evolution in the sexes. Sex differences should result from asymmetries between the sexes in selection or genetic variation but studies investigating both simultaneously are lacking. Here, we combine a quantitative genetic analysis of body size variation, partitioned into autosomal and sex chromosome contributions and ten generations of experimental evolution to dissect the evolution of sexual body size dimorphism in seed beetles (Callosobruchus maculatus) subjected to sexually antagonistic or sex-limited selection. Female additive genetic variance (VA) was primarily linked to autosomes, exhibiting a strong intersexual genetic correlation with males ([Formula: see text] = 0.926), while X- and Y-linked genes further contributed to the male VA and X-linked genes contributed to female dominance variance. Consistent with these estimates, sexual body size dimorphism did not evolve in response to female-limited selection but evolved by 30-50% under male-limited and sexually antagonistic selection. Remarkably, Y-linked variance alone could change dimorphism by 30%, despite the C. maculatus Y chromosome being small and heterochromatic. Our results demonstrate how the potential for sexual dimorphism to evolve depends on both its underlying genetic basis and the nature of sex-specific selection.

Immigration counter-acts local micro-evolution of a major fitness component: Migration-selection balance in free-living song sparrows.

Ongoing adaptive evolution, and resulting "evolutionary rescue" of declining populations, requires additive genetic variation in fitness. Such variation can be increased by gene flow resulting from immigration, potentially facilitating evolution. But, gene flow could in fact constrain rather than facilitate local adaptive evolution if immigrants have low additive genetic values for local fitness. Local migration-selection balance and micro-evolutionary stasis could then result. However, key quantitative genetic effects of natural immigration, comprising the degrees to which gene flow increases the total local additive genetic variance yet counteracts local adaptive evolutionary change, have not been explicitly quantified in wild populations. Key implications of gene flow for population and evolutionary dynamics consequently remain unclear. Our quantitative genetic analyses of long-term data from free-living song sparrows (Melospiza melodia) show that mean breeding value for local juvenile survival to adulthood, a major component of fitness, increased across cohorts more than expected solely due to drift. Such micro-evolutionary change should be expected given nonzero additive genetic variance and consistent directional selection. However, this evolutionary increase was counteracted by negative additive genetic effects of recent immigrants, which increased total additive genetic variance but prevented a net directional evolutionary increase in total additive genetic value. These analyses imply an approximate quantitative genetic migration-selection balance in a major fitness component, and hence demonstrate a key mechanism by which substantial additive genetic variation can be maintained yet decoupled from local adaptive evolutionary change.

Individuals' expected genetic contributions to future generations, reproductive value, and short-term metrics of fitness in free-living song sparrows (Melospiza melodia).

Appropriately defining and enumerating "fitness" is fundamental to explaining and predicting evolutionary dynamics. Yet, general theoretical concepts of fitness are often hard to translate into quantities that can be measured in wild populations experiencing complex environmental, demographic, genetic, and selective variation. Although the "fittest" entities might be widely understood to be those that ultimately leave most descendants at some future time, such long-term legacies can rarely be measured, impeding evaluation of the degree to which tractable short-term metrics of individual fitness could potentially serve as useful direct proxies. One opportunity for conceptual and empirical convergence stems from the principle of individual reproductive value (V i), here defined as the number of copies of each of an individual's alleles that is expected to be present in future generations given the individual's realized pedigree of descendants. As V i tightly predicts an individual's longer term genetic contribution, quantifying V i provides a tractable route to quantifying what, to date, has been an abstract theoretical fitness concept. We used complete pedigree data from free-living song sparrows (Melospiza melodia) to demonstrate that individuals' expected genetic contributions stabilize within an observed 20-year (i.e. approximately eight generation) time period, allowing estimation of individual V i. Considerable among-individual variation in V i was evident in both sexes. Standard metrics of individual lifetime fitness, comprising lifespan, lifetime reproductive success, and projected growth rate, typically explained less than half the variation. We thereby elucidate the degree to which fitness metrics observed on individuals concur with measures of longer term genetic contributions and consider the degree to which analyses of pedigree structure could provide useful complementary insights into evolutionary outcomes.

Is there indirect selection on female extra-pair reproduction through cross-sex genetic correlations with male reproductive fitness?

One key hypothesis explaining the evolution and persistence of polyandry, and resulting female extra-pair reproduction in socially monogamous systems, is that female propensity for extra-pair reproduction is positively genetically correlated with male reproductive fitness and consequently experiences positive cross-sex indirect selection. However, key genetic correlations have rarely been estimated, especially in free-living populations experiencing natural (co)variation in reproductive strategies and fitness. We used long-term life-history and pedigree data from song sparrows (Melospiza melodia) to estimate the cross-sex genetic correlation between female propensity for extra-pair reproduction and adult male lifetime reproductive success, and thereby test a key hypothesis regarding mating system evolution. There was substantial additive genetic variance in both traits, providing substantial potential for indirect selection on female reproductive strategy. However, the cross-sex genetic correlation was estimated to be close to zero. Such small correlations might arise because male reproductive success achieved through extra-pair paternity was strongly positively genetically correlated with success achieved through within-pair paternity, implying that the same successful males commonly sire offspring produced by polyandrous and monogamous females. Cross-sex indirect selection may consequently have limited capacity to drive evolution of female extra-pair reproduction, or hence underlying polyandry, in systems where multiple routes to paternity success exist.

Sex-specific additive genetic variances and correlations for fitness in a song sparrow (Melospiza melodia) population subject to natural immigration and inbreeding.

Quantifying sex-specific additive genetic variance (VA ) in fitness, and the cross-sex genetic correlation (rA ), is prerequisite to predicting evolutionary dynamics and the magnitude of sexual conflict. Further, quantifying VA and rA in underlying fitness components, and genetic consequences of immigration and resulting gene flow, is required to identify mechanisms that maintain VA in fitness. However, these key parameters have rarely been estimated in wild populations experiencing natural environmental variation and immigration. We used comprehensive pedigree and life-history data from song sparrows (Melospiza melodia) to estimate VA and rA in sex-specific fitness and underlying fitness components, and to estimate additive genetic effects of immigrants alongside inbreeding depression. We found evidence of substantial VA in female and male fitness, with a moderate positive cross-sex rA . There was also substantial VA in male but not female adult reproductive success, and moderate VA in juvenile survival but not adult annual survival. Immigrants introduced alleles with negative additive genetic effects on local fitness, potentially reducing population mean fitness through migration load, but alleviating expression of inbreeding depression. Our results show that VA for fitness can be maintained in the wild, and be broadly concordant between the sexes despite marked sex-specific VA in reproductive success.

Individual repeatability and heritability of divorce in a wild population.

Understanding micro-evolutionary responses of mating systems to contemporary selection requires estimating sex-specific additive genetic variances and cross-sex genetic covariances in key reproductive strategy traits. One key trait comprises the occurrence of divorce versus mate fidelity across sequential reproductive attempts. If divorce represents an evolving behavioural strategy that responds to selection it must have non-zero individual repeatability and heritability, but quantitative estimates from wild populations are scarce. We used 39 years of individual breeding records and pedigree data from free-living song sparrows (Melospiza melodia) to quantify sex-specific permanent individual and additive genetic variances, and hence estimate repeatability and heritability, in liability for divorce. We estimated moderate repeatability among females, but little repeatability among males. Estimates of additive genetic variance were small in both sexes, and the cross-sex genetic covariance was close to zero. Consequently, the total heritability was small but likely non-zero, indicating low potential for micro-evolutionary response to selection. Rapid micro-evolutionary change of divorce rate, therefore, appears unlikely, even if there were substantial fitness benefits of divorce and resulting selection.

Accounting for genetic differences among unknown parents in microevolutionary studies: how to include genetic groups in quantitative genetic animal models.

Quantifying and predicting microevolutionary responses to environmental change requires unbiased estimation of quantitative genetic parameters in wild populations. 'Animal models', which utilize pedigree data to separate genetic and environmental effects on phenotypes, provide powerful means to estimate key parameters and have revolutionized quantitative genetic analyses of wild populations. However, pedigrees collected in wild populations commonly contain many individuals with unknown parents. When unknown parents are non-randomly associated with genetic values for focal traits, animal model parameter estimates can be severely biased. Yet, such bias has not previously been highlighted and statistical methods designed to minimize such biases have not been implemented in evolutionary ecology. We first illustrate how the occurrence of non-random unknown parents in population pedigrees can substantially bias animal model predictions of breeding values and estimates of additive genetic variance, and create spurious temporal trends in predicted breeding values in the absence of local selection. We then introduce 'genetic group' methods, which were developed in agricultural science, and explain how these methods can minimize bias in quantitative genetic parameter estimates stemming from genetic heterogeneity among individuals with unknown parents. We summarize the conceptual foundations of genetic group animal models and provide extensive, step-by-step tutorials that demonstrate how to fit such models in a variety of software programs. Furthermore, we provide new functions in r that extend current software capabilities and provide a standardized approach across software programs to implement genetic group methods. Beyond simply alleviating bias, genetic group animal models can directly estimate new parameters pertaining to key biological processes. We discuss one such example, where genetic group methods potentially allow the microevolutionary consequences of local selection to be distinguished from effects of immigration and resulting gene flow. We highlight some remaining limitations of genetic group models and discuss opportunities for further development and application in evolutionary ecology. We suggest that genetic group methods should no longer be overlooked by evolutionary ecologists, but should become standard components of the toolkit for animal model analyses of wild population data sets.

Direct and indirect genetic and fine-scale location effects on breeding date in song sparrows.

Quantifying direct and indirect genetic effects of interacting females and males on variation in jointly expressed life-history traits is central to predicting microevolutionary dynamics. However, accurately estimating sex-specific additive genetic variances in such traits remains difficult in wild populations, especially if related individuals inhabit similar fine-scale environments. Breeding date is a key life-history trait that responds to environmental phenology and mediates individual and population responses to environmental change. However, no studies have estimated female (direct) and male (indirect) additive genetic and inbreeding effects on breeding date, and estimated the cross-sex genetic correlation, while simultaneously accounting for fine-scale environmental effects of breeding locations, impeding prediction of microevolutionary dynamics. We fitted animal models to 38 years of song sparrow (Melospiza melodia) phenology and pedigree data to estimate sex-specific additive genetic variances in breeding date, and the cross-sex genetic correlation, thereby estimating the total additive genetic variance while simultaneously estimating sex-specific inbreeding depression. We further fitted three forms of spatial animal model to explicitly estimate variance in breeding date attributable to breeding location, overlap among breeding locations and spatial autocorrelation. We thereby quantified fine-scale location variances in breeding date and quantified the degree to which estimating such variances affected the estimated additive genetic variances. The non-spatial animal model estimated nonzero female and male additive genetic variances in breeding date (sex-specific heritabilities: 0·07 and 0·02, respectively) and a strong, positive cross-sex genetic correlation (0·99), creating substantial total additive genetic variance (0·18). Breeding date varied with female, but not male inbreeding coefficient, revealing direct, but not indirect, inbreeding depression. All three spatial animal models estimated small location variance in breeding date, but because relatedness and breeding location were virtually uncorrelated, modelling location variance did not alter the estimated additive genetic variances. Our results show that sex-specific additive genetic effects on breeding date can be strongly positively correlated, which would affect any predicted rates of microevolutionary change in response to sexually antagonistic or congruent selection. Further, we show that inbreeding effects on breeding date can also be sex specific and that genetic effects can exceed phenotypic variation stemming from fine-scale location-based variation within a wild population.

Variation in parent-offspring kinship in socially monogamous systems with extra-pair reproduction and inbreeding.

Female extra-pair reproduction in socially monogamous systems is predicted to cause cuckolded socially-paired males to conditionally reduce paternal care, causing selection against extra-pair reproduction and underlying polyandry. However, existing models and empirical studies have not explicitly considered that cuckolded males might be related to their socially-paired female and/or to her extra-pair mate, and therefore be related to extra-pair offspring that they did not sire but could rear. Selection against paternal care, and hence against extra-pair reproduction, might then be weakened. We derive metrics that quantify allele-sharing between within-pair and extra-pair offspring and their mother and her socially-paired male in terms of coefficients of kinship and inbreeding. We use song sparrow (Melospiza melodia) paternity and pedigree data to quantify these metrics, and thereby quantify the joint effects of extra-pair reproduction and inbreeding on a brood's total allelic value to its socially-paired parents. Cuckolded male song sparrows were almost always detectably related to extra-pair offspring they reared. Consequently, although brood allelic value decreased substantially following female extra-pair reproduction, this decrease was reduced by within-pair and extra-pair reproduction among relatives. Such complex variation in kinship within nuclear families should be incorporated into models considering coevolutionary dynamics of extra-pair reproduction, parental care, and inbreeding.

Is Pairing with a Relative Heritable? Estimating Female and Male Genetic Contributions to the Degree of Biparental Inbreeding in Song Sparrows (Melospiza melodia).

The degree of inbreeding expressed within populations can profoundly shape evolutionary dynamics. The degree to which individuals inbreed is frequently assumed to evolve in response to selection, for example, resulting from inbreeding depression. Such evolutionary responses require additive genetic variance (VA) in the degree to which individuals inbreed. However, the magnitude of VA in the degree of biparental inbreeding has never been estimated. We devised a quantitative genetic model to estimate sex-specific VA in the degree to which individuals inbreed while accounting for effects of individuals' own coefficients of inbreeding and genetic effects stemming from immigration. We applied this model to the degree of inbreeding expressed through social pairing in free-living song sparrows (Melospiza melodia). Estimates of VA for both sexes appreciably exceeded 0 and the cross-sex genetic covariance was strongly positive, creating substantial total VA in the degree of inbreeding. Our analyses also revealed inbreeding depression in the degree of inbreeding, such that more inbred individuals paired with closer relatives, and immigrant effects, such that individuals with greater genomic contributions from immigrants paired with more distant relatives. We thereby demonstrate that the degree of biparental inbreeding can show substantial VA in nature and might consequently evolve in response to selection.

Evolution of the additive genetic variance-covariance matrix under continuous directional selection on a complex behavioural phenotype.

Given the pace at which human-induced environmental changes occur, a pressing challenge is to determine the speed with which selection can drive evolutionary change. A key determinant of adaptive response to multivariate phenotypic selection is the additive genetic variance-covariance matrix ( G: ). Yet knowledge of G: in a population experiencing new or altered selection is not sufficient to predict selection response because G: itself evolves in ways that are poorly understood. We experimentally evaluated changes in G: when closely related behavioural traits experience continuous directional selection. We applied the genetic covariance tensor approach to a large dataset (n = 17 328 individuals) from a replicated, 31-generation artificial selection experiment that bred mice for voluntary wheel running on days 5 and 6 of a 6-day test. Selection on this subset of G: induced proportional changes across the matrix for all 6 days of running behaviour within the first four generations. The changes in G: induced by selection resulted in a fourfold slower-than-predicted rate of response to selection. Thus, selection exacerbated constraints within G: and limited future adaptive response, a phenomenon that could have profound consequences for populations facing rapid environmental change.

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."

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.

Are we underestimating the genetic variances of dimorphic traits?

Populations often contain discrete classes or morphs (e.g., sexual dimorphisms, wing dimorphisms, trophic dimorphisms) characterized by distinct patterns of trait expression. In quantitative genetic analyses, the different morphs can be considered as different environments within which traits are expressed. Genetic variances and covariances can then be estimated independently for each morph or in a combined analysis. In the latter case, morphs can be considered as separate environments in a bivariate analysis or entered as fixed effects in a univariate analysis. Although a common approach, we demonstrate that the latter produces downwardly biased estimates of additive genetic variance and heritability unless the quantitative genetic architecture of the traits concerned is perfectly correlated between the morphs. This result is derived for four widely used quantitative genetic variance partitioning methods. Given that theory predicts the evolution of genotype-by-environment (morph) interactions as a consequence of selection favoring different trait combinations in each morph, we argue that perfect correlations between the genetic architectures of the different morphs are unlikely. A sampling of the recent literature indicates that the majority of researchers studying traits expressed in different morphs recognize this and do estimate morph-specific quantitative genetic architecture. However, ca. 16% of the studies in our sample utilized only univariate, fixed-effects models. We caution against this approach and recommend that it be used only if supported by evidence that the genetic architectures of the different morphs do not differ.

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 female's 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.

Limits to behavioral evolution: the quantitative genetics of a complex trait under directional selection.

Replicated selection experiments provide a powerful way to study how "multiple adaptive solutions" may lead to differences in the quantitative-genetic architecture of selected traits and whether this may translate into differences in the timing at which evolutionary limits are reached. We analyze data from 31 generations (n=17,988) of selection on voluntary wheel running in house mice. The rate of initial response, timing of selection limit, and height of the plateau varied significantly between sexes and among the four selected lines. Analyses of litter size and realized selection differentials seem to rule out counterposing natural selection as a cause of the selection limits. Animal-model analyses showed that although the additive genetic variance was significantly lower in selected than control lines, both before and after the limits, the decrease was not sufficient to explain the limits. Moreover, directional selection promoted a negative covariance between additive and maternal genetic variance over the first 10 generations. These results stress the importance of replication in selection studies of higher-level traits and highlight the fact that long-term predictions of response to selection are not necessarily expected to be linear because of the variable effects of selection on additive genetic variance and maternal effects.