Abundance, rarity and invasion debt among exotic species in a patchy ecosystem

Community assembly through species invasions is a long-term process, for which vital information regarding future trends can be contained in current patterns. Using comparative analyses of native and exotic plant assemblages from meadow patches on islands in British Columbia, Canada, we examined multiple lines of evidence for ‘invasion debt’, a latent expansion of exotic species populations. We show that: (1) short-dispersing species are underrepresented compared to their long-dispersing counterparts in exotic species only; (2) among species that are invasive elsewhere in North America, a greater proportion of long dispersers are common in the study area and a greater proportion of short dispersers are rare; and (3) time since arrival in the study region is positively related to number of occurrences in exotic species. In addition, we show that a suite of exotic species possesses the facility of rapid long-distance dispersal and ability to establish viable populations on even the most isolated and least disturbed patches. While some highly-dispersive exotic species can rapidly colonize new areas, short dispersers appear to exhibit invasion debt, with their potential distributions only being realized in the long term. Removing or even reducing populations of many rapid colonizers could be extremely difficult; however, for species exhibiting patterns most consistent with invasion debt, an opportunity exists for monitoring and removal to help reduce potential competition with native species.     

PEDIGREE ERROR DUE TO EXTRA‐PAIR REPRODUCTION SUBSTANTIALLY BIASES ESTIMATES OF INBREEDING DEPRESSION

Understanding the evolutionary dynamics of inbreeding and inbreeding depression requires unbiased estimation of inbreeding depression across diverse mating systems. However, studies estimating inbreeding depression often measure inbreeding with error, for example, based on pedigree data derived from observed parental behavior that ignore paternity error stemming from multiple mating. Such paternity error causes error in estimated coefficients of inbreeding (f) and reproductive success and could bias estimates of inbreeding depression. We used complete “apparent” pedigree data compiled from observed parental behavior and analogous “actual” pedigree data comprising genetic parentage to quantify effects of paternity error stemming from extra‐pair reproduction on estimates of f, reproductive success, and inbreeding depression in free‐living song sparrows (Melospiza melodia). Paternity error caused widespread error in estimates of f and male reproductive success, causing inbreeding depression in male and female annual and lifetime reproductive success and juvenile male survival to be substantially underestimated. Conversely, inbreeding depression in adult male survival tended to be overestimated when paternity error was ignored. Pedigree error stemming from extra‐pair reproduction therefore caused substantial and divergent bias in estimates of inbreeding depression that could bias tests of evolutionary theories regarding inbreeding and inbreeding depression and their links to variation in mating system.     

Breeding experience and population density affect the ability of a songbird to respond to future climate variation

Predicting how populations respond to climate change requires an understanding of whether individuals or cohorts within populations vary in their response to climate variation. We used mixed-effects models on a song sparrow (Melospiza melodia) population in British Columbia, Canada, to examine differences among females and cohorts in their average breeding date and breeding date plasticity in response to the El Niño Southern Oscillation. Climatic variables, age and population density were strong predictors of timing of breeding, but we also found considerable variation among individual females and cohorts. Within cohorts, females differed markedly in their breeding date and cohorts also differed in their average breeding date and breeding date plasticity. The plasticity of a cohort appeared to be due primarily to an interaction between the environmental conditions (climate and density) experienced at different ages rather than innate inter-cohort differences. Cohorts that expressed higher plasticity in breeding date experienced warmer El Niño springs in their second or third breeding season, suggesting that prior experience affects how well individuals responded to abnormal climatic conditions. Cohorts born into lower density populations also expressed higher plasticity in breeding date. Interactions between age, experience and environmental conditions have been reported previously for long-lived taxa. Our current results indicate that similar effects operate in a short-lived, temperate songbird.     

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.     

Micro-spatial genetic structure in song sparrows (<Emphasis Type="Italic">Melospiza melodia</Emphasis>)

The spatial genetic structure of populations is strongly influenced by current and historical patterns of gene flow and drift, which in the simplest case, is limited by geographic distance. We examined the microspatial genetic structure within 33 populations of song sparrows (Melospiza melodia) which included eight subspecies located across coastal areas in southern British Columbia (BC) and California. We also examined the effect of water barriers and local density estimates on genetic structuring. Across both regions, positive genetic structure was detectable at distances of less than 10 km. Genetic divergence was highest in Californian subspecies, perhaps due to reduced gene flow across sub-specific contact zones. In BC, populations distributed across islands displayed greater genetic structuring over similar spatial scales than those across mainland sites, supporting the prediction that water barriers reduce gene flow in this species. Our results confirm both the expectation for fine-scale genetic structure in these generally sedentary subspecies, and the role of landscape features in generating geographic variation in genetic structure.     

Hamilton and Zuk meet heterozygosity? Song repertoire size indicates inbreeding and immunity in song sparrows (Melospiza melodia)

Hamilton and Zuk's influential hypothesis of parasite-mediated sexual selection proposes that exaggerated secondary sexual ornaments indicate a male's addictive genetic immunity to parasites. However, genetic correlated of ornaments and immunity have rarely been explicitly identified. Evidence supporting Hamilton and Zuk's hypothesis has instead been gathered by looking for positive phenotypic correlations between ornamentation and immunity; such correlations are assumed to reflect causal, addictive relationships between these traits. We show that in a song sparrows, Melospiza melodia, male's song repertoire size, a secondary sexual trait, increased with his cell-mediated immune response (CMI) to an experimental challenge. However, this phenotypic correlation could be explained because both repertoire size and CMI declined with a male's inbreeding level. Repertoire size therefore primarily indicated a male's relative heterozygosity, a non-addictive genetic predictor of immunity. Caution may therefore be required when interpreting phenotypic correlations as support for Hamilton and Zuk's addictive model of sexual selection. However, our results suggest that female song sparrows choosing with large repertoires would on average acquire more outbred and therefore more heterozygous mates. Such genetic dominance effects on ornamentation are likely to influence evolutionary trajectories of female choice, and should be explicitly incorporated into genetic models of sexual selection.     

Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population

1. Conservation biologists are concerned about the interactive effects of environmental stress and inbreeding because such interactions could affect the dynamics and extinction risk of small and isolated populations, but few studies have tested for these interactions in nature. 2. We used data from the long-term population study of song sparrows Melospiza melodia on Mandarte Island to examine the joint effects of inbreeding and environmental stress on four fitness traits that are known to be affected by the inbreeding level of adult birds: hatching success, laying date, male mating success and fledgling survival. 3. We found that inbreeding depression interacted with environmental stress to reduce hatching success in the nests of inbred females during periods of rain. 4. For laying date, we found equivocal support for an interaction between parental inbreeding and environmental stress. In this case, however, inbred females experienced less inbreeding depression in more stressful, cooler years. 5. For two other traits, we found no evidence that the strength of inbreeding depression varied with environmental stress. First, mated males fathered fewer nests per season if inbred or if the ratio of males to females in the population was high, but inbreeding depression did not depend on sex ratio. Second, fledglings survived poorly during rainy periods and if their father was inbred, but the effects of paternal inbreeding and rain did not interact. 6. Thus, even for a single species, interactions between the inbreeding level and environmental stress may not occur in all traits affected by inbreeding depression, and interactions that do occur will not always act synergistically to further decrease fitness.     

Are there indirect fitness benefits of female extra-pair reproduction? Lifetime reproductive success of within-pair and extra-pair offspring

The forces driving extra-pair reproduction by socially monogamous females, and the resulting genetic polyandry, remain unclear. A testable prediction of the hypothesis that extra-pair reproduction partly reflects indirect selection on females is that extra-pair young (EPY) will be fitter than their within-pair young (WPY) maternal half-siblings. This prediction has not been comprehensively tested in a wild population, requiring data on the lifetime reproductive success (LRS) of maternal half-sib EPY and WPY. We used 17 years of genetic parentage data from song sparrows, Melospiza melodia, to compare the LRS of hatched EPY and WPY maternal half-siblings measured as their lifetime number of hatched offspring, recruited offspring, and hatched grandoffspring. EPY hatchlings were not significantly fitter than WPY hatchlings for any of three measures of LRS. Furthermore, opposite to prediction, EPY hatchlings tended to have lower LRS than their maternal half-sibling WPY hatchlings on average. EPY also tended to be less likely to survive to hatch than their maternal half-sibling WPY. Taken together, these results fail to support one key hypothesis explaining the evolution of genetic polyandry by socially monogamous females and suggest there may be weak indirect selection against female extra-pair reproduction in song sparrows.     

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.