Multi-generation genetic contributions of immigrants reveal cryptic elevated and sex-biased effective gene flow within a natural meta-population.

Impacts of immigration on micro-evolution and population dynamics fundamentally depend on net rates and forms of resulting gene flow into recipient populations. Yet, the degrees to which observed rates and sex ratios of physical immigration translate into multi-generational genetic legacies have not been explicitly quantified in natural meta-populations, precluding inference on how movements translate into effective gene flow and eco-evolutionary outcomes. Our analyses of three decades of complete song sparrow (Melospiza melodia) pedigree data show that multi-generational genetic contributions from regular natural immigrants substantially exceeded those from contemporary natives, consistent with heterosis-enhanced introgression. However, while contributions from female immigrants exceeded those from female natives by up to three-fold, male immigrants' lineages typically went locally extinct soon after arriving. Both the overall magnitude, and the degree of female bias, of effective gene flow therefore greatly exceeded those which would be inferred from observed physical arrivals, altering multiple eco-evolutionary implications of immigration.

Multigenerational Fitness Effects of Natural Immigration Indicate Strong Heterosis and Epistatic Breakdown in a Wild Bird Population.

AbstractThe fitness of immigrants and their descendants produced within recipient populations fundamentally underpins the genetic and population dynamic consequences of immigration. Immigrants can in principle induce contrasting genetic effects on fitness across generations, reflecting multifaceted additive, dominance, and epistatic effects. Yet full multigenerational and sex-specific fitness effects of regular immigration have not been quantified within naturally structured systems, precluding inference on underlying genetic architectures and population outcomes. We used four decades of song sparrow (Melospiza melodia) life history and pedigree data to quantify fitness of natural immigrants, natives, and their F1, F2, and backcross descendants and test for evidence of nonadditive genetic effects. Values of key fitness components (including adult lifetime reproductive success and zygote survival) of F1 offspring of immigrant-native matings substantially exceeded their parent mean, indicating strong heterosis. Meanwhile, F2 offspring of F1-F1 matings had notably low values, indicating surprisingly strong epistatic breakdown. Furthermore, magnitudes of effects varied among fitness components and differed between female and male descendants. These results demonstrate that strong nonadditive genetic effects on fitness can arise within weakly structured and fragmented populations experiencing frequent natural immigration. Such effects will substantially affect the net degree of effective gene flow and resulting local genetic introgression and adaptation.

Immune genotypes, immune responses, and survival in a wild bird population.

Individuals vary in their immune genotype, inbreeding coefficient f, immune responses, survival to adulthood, and adult longevity. However, whether immune genes predict survival or longevity, whether such relationships are mediated through immune responses, and how f affects immune genotype remain unclear. We use a wild song sparrow (Melospiza melodia) population in which survival to adulthood, adult longevity, and f were measured precisely, and in which immune responses have previously been assessed. We investigate four toll-like receptor (TLR) and the major histocompatibility complex (MHC) class IIB exon 2 genes. We test whether immune genes predict fitness (survival to adulthood or adult longevity); whether immune genes predict immune response; whether immune response predicts fitness and whether fitness, immune responses, or immune genotypes are correlated with f. We find that survival to adulthood is not associated with immune gene variation, but adult longevity is decreased by high MHC allele diversity (especially in birds that were relatively outbred), and by the presence of a specific MHC supertype. Immune responses were affected by specific immune genotypes. Survival to adulthood and adult longevity were not predicted by immune response, implying caution in the use of immune response as a predictor for fitness. We also found no relationship between f and immune genotype. This finding indicates that immune gene associations with longevity and immune response are not artefacts of f, and suggests that pathogen-mediated selection at functional loci can slow the loss of genetic variation arising from genetic drift and small population size.

Adaptation to climate change through seasonal migration revealed by climatic versus demographic niche models.

Predicting the geographic range of species and their response to climatic variation and change are entwined goals in conservation and evolutionary ecology. Species distribution models (SDMs) are foundational in this effort and used to visualize the geographic range of species as the spatial representation of its realized niche. SDMs are also used to forecast range shifts under climate change, but often in the absence of empirical evidence that climate limits population growth. We explored the influence of climate on demography, seasonal migration, and the extent of the geographic range in song sparrows (Melospiza melodia), a species thought to display marked local adaptation to regional climate. To do so, we developed SDMs to predict the demographic and climate niches of migratory and resident song sparrows across our study area in western North America from California to Alaska, using 48 years of demographic data from a focal population in British Columbia and 1.2 million continental-scale citizen science observations. Spatial agreement of our demographic and climate niche models in the region of our focal population was strong (76%), supporting the hypothesis that demographic performance and the occurrence of seasonal migration varied predictably with climatic conditions. In contrast, agreement at the northern (58%) and southern (40%) extents of our study area was lower, as expected if the factors limiting population growth vary regionally. Our results support the hypothesis that local climate drives spatial variation in the occurrence of seasonal migration in song sparrows by limiting the fitness of year-round residents, and suggest that climate warming has favored range expansions and facilitated an upward shift in elevational range song sparrows that forgo seasonal migration. Our work highlights the potential role of seasonal migration in climate adaptation and limits on the reliability of climate niche models not validated with demographic data.

Are immigrants outbred and unrelated? Testing standard assumptions in a wild metapopulation.

Immigration into small recipient populations is expected to alleviate inbreeding and increase genetic variation, and hence facilitate population persistence through genetic and/or evolutionary rescue. Such expectations depend on three standard assumptions: that immigrants are outbred, unrelated to existing natives at arrival, and unrelated to each other. These assumptions are rarely explicitly verified, including in key field systems in evolutionary ecology. Yet, they could be violated due to non-random or repeated immigration from adjacent small populations. We combined molecular genetic marker data for 150-160 microsatellite loci with comprehensive pedigree data to test the three assumptions for a song sparrow (Melospiza melodia) population that is a model system for quantifying effects of inbreeding and immigration in the wild. Immigrants were less homozygous than existing natives on average, with mean homozygosity that closely resembled outbred natives. Immigrants can therefore be considered outbred on the focal population scale. Comparisons of homozygosity of real or hypothetical offspring of immigrant-native, native-native and immigrant-immigrant pairings implied that immigrants were typically unrelated to existing natives and to each other. Indeed, immigrants' offspring would be even less homozygous than outbred individuals on the focal population scale. The three standard assumptions of population genetic and evolutionary theory were consequently largely validated. Yet, our analyses revealed some deviations that should be accounted for in future analyses of heterosis and inbreeding depression, implying that the three assumptions should be verified in other systems to probe patterns of non-random or repeated dispersal and facilitate precise and unbiased estimation of key evolutionary parameters.

Genomic differentiation and local adaptation on a microgeographic scale in a resident songbird.

Elucidating forces capable of driving species diversification in the face of gene flow remains a key goal in evolutionary biology. Song sparrows, Melospiza melodia, occur as 25 subspecies in diverse habitats across North America, are among the continent's most widespread vertebrate species, and are exemplary of many highly variable species for which the conservation of locally adapted populations may be critical to their range-wide persistence. We focus here on six morphologically distinct subspecies resident in the San Francisco Bay region, including three salt-marsh endemics and three residents in upland and riparian habitats adjacent to the Bay. We used reduced-representation sequencing to generate 2,773 SNPs to explore genetic differentiation, spatial population structure, and demographic history. Clustering separated individuals from each of the six subspecies, indicating subtle differentiation at microgeographic scales. Evidence of limited gene flow and low nucleotide diversity across all six subspecies further supports a hypothesis of isolation among locally adapted populations. We suggest that natural selection for genotypes adapted to salt marsh environments and changes in demography over the past century have acted in concert to drive the patterns of diversification reported here. Our results offer evidence of microgeographic specialization in a highly polytypic bird species long discussed as a model of sympatric speciation and rapid adaptation, and they support the hypothesis that conserving locally adapted populations may be critical to the range-wide persistence of similarly highly variable species.

Testing predictions of inclusive fitness theory in inbreeding relatives with biparental care.

Inclusive fitness theory predicts that parental care will vary with relatedness between potentially caring parents and offspring, potentially shaping mating system evolution. Systems with extra-pair paternity (EPP), and hence variable parent-brood relatedness, provide valuable opportunities to test this prediction. However, existing theoretical and empirical studies assume that a focal male is either an offspring's father with no inbreeding, or is completely unrelated. We highlight that this simple dichotomy does not hold given reproductive interactions among relatives, complicating the effect of EPP on parent-brood relatedness yet providing new opportunities to test inclusive fitness theory. Accordingly, we tested hierarchical hypotheses relating parental feeding rate to parent-brood relatedness, parent kinship and inbreeding, using song sparrows (Melospiza melodia) experiencing natural variation in relatedness. As predicted, male and female feeding rates increased with relatedness to a dependent brood, even controlling for brood size. Male feeding rate tended to decrease as paternity loss increased, and increased with increasing kinship and hence inbreeding between socially paired mates. We thereby demonstrate that variation in a key component of parental care concurs with subtle predictions from inclusive fitness theory. We additionally highlight that such effects can depend on the underlying social mating system, potentially generating status-specific costs of extra-pair reproduction.

The Consequences of Polyandry for Sibship Structures, Distributions of Relationships and Relatedness, and Potential for Inbreeding in a Wild Population.

The evolutionary benefits of simultaneous polyandry (female multiple mating within a single reproductive event) remain elusive. One potential benefit could arise if polyandry alters sibship structures and consequent relationships and relatedness among females' descendants, thereby intrinsically reducing future inbreeding risk (the indirect inbreeding avoidance hypothesis). However such effects have not been quantified in naturally complex mating systems that also encompass iteroparity, overlapping generations, sequential polyandry, and polygyny. We used long-term social and genetic pedigree data from song sparrows (Melospiza melodia) to quantify cross-generational consequences of simultaneous polyandry for offspring sibship structures and distributions of relationships and relatedness among possible mates. Simultaneous polyandry decreased full sibships and increased half-sibships, on average, but such effects varied among females and were smaller than would occur in the absence of sequential polyandry or polygyny. Further, while simultaneous polyandry decreased the overall frequencies of possible matings among adult full sibs, it increased the frequencies of possible matings among adult half-sibs and more distant relatives. These results imply that the intrinsic consequences of simultaneous polyandry for inbreeding risk could cause weak indirect selection on polyandry, but the magnitude and direction of such effects will depend on complex interactions with other mating system components and the form of inbreeding depression.

Individual fitness and the effects of a changing climate on the cessation and length of the breeding period using a 34-year study of a temperate songbird.

Studies of the phenological responses of animals to climate change typically emphasize the initiation of breeding although climatic effects on the cessation and length of the breeding period may be as or more influential of fitness. We quantified links between climate, the cessation and length of the breeding period, and individual survival and reproduction using a 34-year study of a resident song sparrow (Melospiza melodia) population subject to dramatic variation in climate. We show that the cessation and length of the breeding period varied strongly across years, and predicted female annual fecundity but not survival. Breeding period length was more influential of fecundity than initiation or cessation of breeding alone. Warmer annual temperature and drier winters and summers predicted an earlier cessation of breeding. Population density, the date breeding was initiated, a female's history of breeding success, and the number of breeding attempts initiated previously also predicted the cessation of breeding annually, indicating that climatic, population, and individual factors may interact to affect breeding phenology. Linking climate projections to our model results suggests that females will both initiate and cease breeding earlier in the future; this will have opposite effects on individual reproductive rate because breeding earlier is expected to increase fecundity, whereas ceasing breeding earlier should reduce it. Identifying factors affecting the cessation and length of the breeding period in multiparous species may be essential to predicting individual fitness and population demography. Given a rich history of studies on the initiation of breeding in free-living species, re-visiting those data to estimate climatic effects on the cessation and length of breeding should improve our ability to predict the impacts of climate change on multiparous species.

Purifying Selection in the Toll-Like Receptors of Song Sparrows Melospiza melodia.

Variation in immune gene sequences is known to influence resistance to infectious diseases and parasites, and hence survival and mate choice, across animal taxa. Toll-like receptors (TLRs) comprise one essential gene family in the vertebrate innate immune system and recognize evolutionarily conserved structures from all major microorganism classes. However, the causes and consequences of TLR variation in passerine birds remain largely unexplored. We examined 7 TLR genes in song sparrows (Melospiza melodia), a species that is studied across North America. We then examined sequences from 4 unduplicated TLRs (TLR1LB, TLR3, TLR4, and TLR15) from birds in 2 parts of the species' range (N = 27, N = 6), tested for evidence of selection, and conducted pilot analyses of the role of TLR heterozygosity in survival. We identified 45 SNPs: 19 caused changes in amino acid sequences and 2 of these were likely deleterious. We found no evidence of codon-level episodic positive selection but detected purifying selection at codons in all TLRs. Contrary to expectations we found no strong correlation between heterozygosity at TLRs and inbreeding coefficient f (estimate ± standard error [SE] = -0.68 ± 0.37, Radj2 = 0.08, F1,25 = 3.38, P = 0.08). In addition, pilot analyses revealed no relationship between TLR heterozygosity and survival (ß ± SE: 0.09 ± 2.00, P = 0.96), possibly due to small sample size. Further analyses of genetic diversity in TLRs are likely to advance understanding of the effects of innate immune gene diversity on the fitness and persistence of wild populations.

Pedigree-based inbreeding coefficient explains more variation in fitness than heterozygosity at 160 microsatellites in a wild bird population.

Although the pedigree-based inbreeding coefficient F predicts the expected proportion of an individual's genome that is identical-by-descent (IBD), heterozygosity at genetic markers captures Mendelian sampling variation and thereby provides an estimate of realized IBD. Realized IBD should hence explain more variation in fitness than their pedigree-based expectations, but how many markers are required to achieve this in practice remains poorly understood. We use extensive pedigree and life-history data from an island population of song sparrows (Melospiza melodia) to show that the number of genetic markers and pedigree depth affected the explanatory power of heterozygosity and F, respectively, but that heterozygosity measured at 160 microsatellites did not explain more variation in fitness than F This is in contrast with other studies that found heterozygosity based on far fewer markers to explain more variation in fitness than F Thus, the relative performance of marker- and pedigree-based estimates of IBD depends on the quality of the pedigree, the number, variability and location of the markers employed, and the species-specific recombination landscape, and expectations based on detailed and deep pedigrees remain valuable until we can routinely afford genotyping hundreds of phenotyped wild individuals of genetic non-model species for thousands of genetic markers.

Age and years to death disparately influence reproductive allocation in a short-lived bird.

Theory predicts that reproduction will change as individuals near the end of their lives by either increasing reproductive allocation (terminal allocation hypothesis) or decreasing allocation (senescence hypothesis) toward the end of life. Although senescence has received more support, few studies examine how both age and years to death influence late-life reproduction. We used a 37-yr study of Song Sparrows (Melospiza melodia) to ask how age and years to death influenced reproductive allocation late in life. We observed both senescence and terminal allocation, and that age and years to death interacted to influence individual variation in allocation tactics. In particular, we observed a decline in allocation in older individuals (senescence), but only when comparing individuals with the same number of years to death. Likewise, we observed terminal allocation, but only in young females. Reproductive tactics were most variable in young females, with many exerting high effort but living 1-2 yr, and others exerting low effort annually and living longer. Our results suggest that late-life reproductive tactics are influenced by both chronological age and years to death, and that short- and long-lived females with differing reproductive tactics exist within this population of Song Sparrows.

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.

Changing gull diet in a changing world: a 150-year stable isotope (δ13C, δ15N) record from feathers collected in the Pacific Northwest of North America.

The world's oceans have undergone significant ecological changes following European colonial expansion and associated industrialization. Seabirds are useful indicators of marine food web structure and can be used to track multidecadal environmental change, potentially reflecting long-term human impacts. We used stable isotope (δ(13)C, δ(15)N) analysis of feathers from glaucous-winged gulls (Larus glaucescens) in a heavily disturbed region of the northeast Pacific to ask whether diets of this generalist forager changed in response to shifts in food availability over 150 years, and whether any detected change might explain long-term trends in gull abundance. Sampled feathers came from birds collected between 1860 and 2009 at nesting colonies in the Salish Sea, a transboundary marine system adjacent to Washington, USA and British Columbia, Canada. To determine whether temporal trends in stable isotope ratios might simply reflect changes to baseline environmental values, we also analysed muscle tissue from forage fishes collected in the same region over a multidecadal timeframe. Values of δ(13)C and δ(15)N declined since 1860 in both subadult and adult gulls (δ(13)C, ~ 2-6‰; δ(15)N, ~4-5‰), indicating that their diet has become less marine over time, and that birds now feed at a lower trophic level than previously. Conversely, forage fish δ(13)C and δ(15)N values showed no trends, supporting our conclusion that gull feather values were indicative of declines in marine food availability rather than of baseline environmental change. Gradual declines in feather isotope values are consistent with trends predicted had gulls consumed less fish over time, but were equivocal with respect to whether gulls had switched to a more garbage-based diet, or one comprising marine invertebrates. Nevertheless, our results suggest a long-term decrease in diet quality linked to declining fish abundance or other anthropogenic influences, and may help to explain regional population declines in this species and other piscivores.

Double decomposition: decomposing the variance in subcomponents of male extra-pair reproductive success.

1. Extra-pair reproductive success (EPRS) is a key component of male fitness in socially monogamous systems and could cause selection on female extra-pair reproduction if extra-pair offspring (EPO) inherit high value for EPRS from their successful extra-pair fathers. However, EPRS is itself a composite trait that can be fully decomposed into subcomponents of variation, each of which can be further decomposed into genetic and environmental variances. However, such decompositions have not been implemented in wild populations, impeding evolutionary inference. 2. We first show that EPRS can be decomposed into the product of three life-history subcomponents: the number of broods available to a focal male to sire EPO, the male's probability of siring an EPO in an available brood and the number of offspring in available broods. This decomposition of EPRS facilitates estimation from field data because all subcomponents can be quantified from paternity data without need to quantify extra-pair matings. Our decomposition also highlights that the number of available broods, and hence population structure and demography, might contribute substantially to variance in male EPRS and fitness. 3. We then used 20 years of complete genetic paternity and pedigree data from wild song sparrows (Melospiza melodia) to partition variance in each of the three subcomponents of EPRS, and thereby estimate their additive genetic variance and heritability conditioned on effects of male coefficient of inbreeding, age and social status. 4. All three subcomponents of EPRS showed some degree of within-male repeatability, reflecting combined permanent environmental and genetic effects. Number of available broods and offspring per brood showed low additive genetic variances. The estimated additive genetic variance in extra-pair siring probability was larger, although the 95% credible interval still converged towards zero. Siring probability also showed inbreeding depression and increased with male age, while the numbers of available broods and offspring per brood did not. 5. Our results indicate that the probability that a male will sire an EPO in an available brood is the primary source of genetic variation in male EPRS, implying that the evolution of female extra-pair reproduction could be facilitated by genetic covariance with this subcomponent of EPRS.

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.

Human-Induced Long-Term Shifts in Gull Diet from Marine to Terrestrial Sources in North America's Coastal Pacific: More Evidence from More Isotopes (δ2H, δ34S).

Measurements of naturally occurring stable isotopes in tissues of seabirds and their prey are a powerful tool for investigating long-term changes in marine foodwebs. Recent isotopic (δ(15)N, δ(13)C) evidence from feathers of Glaucous-winged Gulls (Larus glaucescens) has shown that over the last 150 years, this species shifted from a midtrophic marine diet to one including lower trophic marine prey and/or more terrestrial or freshwater foods. However, long-term isotopic patterns of δ(15)N and δ(13)C cannot distinguish between the relative importance of lower trophic-level marine foods and terrestrial sources. We examined 48 feather stable-hydrogen (δ(2)H) and -sulfur (δ(34)S) isotope values from this same 150-year feather set and found additional isotopic evidence supporting the hypothesis that gulls shifted to terrestrial and/or freshwater prey. Mean feather δ(2)H and δ(34)S values (± SD) declined from the earliest period (1860-1915; n = 12) from -2.5 ± 21.4 ‰ and 18.9 ± 2.7 ‰, respectively, to -35.5 ± 15.5 ‰ and 14.8 ± 2.4 ‰, respectively, for the period 1980-2009 (n = 12). We estimated a shift of ∼ 30% increase in dependence on terrestrial/freshwater sources. These results are consistent with the hypothesis that gulls increased terrestrial food inputs in response to declining forage fish availability.

Distinguishing individual quality from habitat preference and quality in a territorial passerine.

Theory predicts that animals breeding in heterogeneous landscapes preferentially occupy habitats likely to maximize individual fitness, but identifying those habitats has proved problematic. Many studies develop metrics of habitat quality linked to site-specific reproductive output measured in successive years, but few separate the independent effects of individual "intrinsic quality" from those due solely to the attributes of the habitats themselves. In many populations, processes such as competitive territory defense, longevity, site-fidelity, and variation in breeding density and territory size over time have the potential to limit the degree to which individual and habitat quality will be positively related in nature. However, the effects of these processes on estimates of habitat or site-specific reproductive output have not been thoroughly investigated. We show that, in an insular population of Song Sparrows (Melospiza melodia), females nested preferentially in breeding sites with high mean reproductive output assessed over 35 years, and that variation in site-specific reproductive output was positively related to female intrinsic quality, measured here as the lifetime reproductive success of individual females relative to others hatched the same year (rLRS). In contrast, vegetation traits (shrub cover, edge, and soil depth) predicted female preference for breeding sites but did not predict site-specific variation in annual reproductive output. Female quality also did not predict which females occupied more- or less-preferred breeding sites over the study period. However, mean annual reproductive output of breeding sites estimated over 35 years was strongly positively related to the quality of the females that nested in them. Overall, these results indicate that site-specific estimates of habitat quality that do not consider the quality of the individuals occupying those sites may include substantial bias due to variation in occupant quality, and thus may not reliably predict the intrinsic effects of habitat quality on individual or population fitness.

Decomposing variation in male reproductive success: age-specific variances and covariances through extra-pair and within-pair reproduction.

Age-specific variances and covariances in reproductive success shape the total variance in lifetime reproductive success (LRS), age-specific opportunities for selection, and population demographic variance and effective size. Age-specific (co)variances in reproductive success achieved through different reproductive routes must therefore be quantified to predict population, phenotypic and evolutionary dynamics in age-structured populations. While numerous studies have quantified age-specific variation in mean reproductive success, age-specific variances and covariances in reproductive success, and the contributions of different reproductive routes to these (co)variances, have not been comprehensively quantified in natural populations. We applied 'additive' and 'independent' methods of variance decomposition to complete data describing apparent (social) and realised (genetic) age-specific reproductive success across 11 cohorts of socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia). We thereby quantified age-specific (co)variances in male within-pair and extra-pair reproductive success (WPRS and EPRS) and the contributions of these (co)variances to the total variances in age-specific reproductive success and LRS. 'Additive' decomposition showed that within-age and among-age (co)variances in WPRS across males aged 2-4 years contributed most to the total variance in LRS. Age-specific (co)variances in EPRS contributed relatively little. However, extra-pair reproduction altered age-specific variances in reproductive success relative to the social mating system, and hence altered the relative contributions of age-specific reproductive success to the total variance in LRS. 'Independent' decomposition showed that the (co)variances in age-specific WPRS, EPRS and total reproductive success, and the resulting opportunities for selection, varied substantially across males that survived to each age. Furthermore, extra-pair reproduction increased the variance in age-specific reproductive success relative to the social mating system to a degree that increased across successive age classes. This comprehensive decomposition of the total variances in age-specific reproductive success and LRS into age-specific (co)variances attributable to two reproductive routes showed that within-age and among-age covariances contributed substantially to the total variance and that extra-pair reproduction can alter the (co)variance structure of age-specific reproductive success. Such covariances and impacts should consequently be integrated into theoretical assessments of demographic and evolutionary processes in age-structured populations.

Human influence and classical biogeographic predictors of rare species occurrence.

Biogeographic theory predicts that rare species occur more often in larger, less-isolated habitat patches and suggests that patch size and connectivity are positive predictors of patch quality for conservation. However, in areas substantially modified by humans, rare species may be relegated to the most isolated patches. We used data from plant surveys of 81 meadow patches in the Georgia Basin of Canada and the United States to show that presence of threatened and endangered plants was positively predicted for patches that were isolated on small islands surrounded by ocean and for patches that were isolated by surrounding forest. Neither patch size nor connectivity were positive predictors of rare species occurrence. Thus, in our study area, human influence, presumably due to disturbance or introduction of competitive non-native species, appears to have overwhelmed classical predictors of rare species distribution, such that greater patch isolation appeared to favor presence of rare species. We suggest conservation planners consider the potential advantages of protecting geographically isolated patches in human-modified landscapes because such patches may represent the only habitats in which rare species are likely to persist.