Jane M. Reid

Identification of 100 fundamental ecological questions

Summary 1. Fundamental ecological research is both intrinsically interesting and provides the basic knowledge required to answer applied questions of importance to the management of the natural world. The 100th anniversary of the British Ecological Society in 2013 is an opportune moment to reflect on the current status of ecology as a science and look forward to high-light priorities for future work.

Inbreeding avoidance, tolerance, or preference in animals?

Animal ecologists commonly assume that the reduced fitness that often afflicts inbred offspring will inevitably cause selection for inbreeding avoidance. Although early empirical studies often reported inbreeding avoidance, recent studies suggest that animals sometimes show no avoidance or even prefer to mate with relatives. However, current theory is insufficient to predict whether animals should avoid, tolerate, or prefer inbreeding and hence to understand overall inbreeding strategy. Furthermore, quantifying inbreeding strategy is challenging, requiring relatedness among unbiased sets of actual and potential mates to be accurately estimated. Here, we highlight key limitations of current theory and empirical tests, and summarise the advances required to predict, quantify, and understand animal inbreeding strategies.

Intrinsic parent-offspring correlation in inbreeding level in a song sparrow (Melospiza melodia) population open to immigration

The extent to which offspring resemble their parents in genotype and phenotype underpins patterns of genetic and phenotypic variation, selection, and evolution in natural populations. Genetic and phenotypic resemblance can clearly result from additive genetic variance and can be shaped by nongenetic parental and common environmental influences. In contrast, there is no straightforward expectation that inbreeding coefficient (f), a nonadditive component of genetic “quality,” should be correlated across parents and offspring in sexually reproducing species or consequently cause resemblance across generations. Here, we report a significant parent f–offspring f correlation within a free‐living pedigreed population of song sparrows (Melospiza melodia) on Mandarte Island, Canada. Across 15 years, relatively inbred parents had relatively inbred offspring on average. We show that rather than requiring nonrandom pairing with respect to f and kinship, parent f–offspring f correlations arise as an intrinsic consequence of random pairing within Mandarte’s open population, where immigrants interbreed with Mandarte‐hatched natives. However, on Mandarte, parent f–offspring f correlations may have been exacerbated because relatively inbred individuals paired with more closely related mates than expected by chance. Such intrinsic parent f–offspring f correlations have major implications for the understanding of resemblance, selection, and evolution in natural populations.

Testing evolutionary models of senescence in a natural population: age and inbreeding effects on fitness components in song sparrows

Mutation accumulation (MA) and antagonistic pleiotropy (AP) have each been hypothesized to explain the evolution of ‘senescence’ or deteriorating fitness in old age. These hypotheses make contrasting predictions concerning age dependence in inbreeding depression in traits that show senescence. Inbreeding depression is predicted to increase with age under MA but not under AP, suggesting one empirical means by which the two can be distinguished. We use pedigree and life-history data from free-living song sparrows (Melospiza melodia) to test for additive and interactive effects of age and individual inbreeding coefficient (f) on fitness components, and thereby assess the evidence for MA. Annual reproductive success (ARS) and survival (and therefore reproductive value) declined in old age in both sexes, indicating senescence in this short-lived bird. ARS declined with f in both sexes and survival declined with f in males, indicating inbreeding depression in fitness. We observed a significant age×f interaction for male ARS (reflecting increased inbreeding depression as males aged), but not for female ARS or survival in either sex. These analyses therefore provide mixed support for MA. We discuss the strengths and limitations of such analyses and therefore the value of natural pedigreed populations in testing evolutionary models of senescence.

Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia)

The consequences of inbreeding for host immunity to parasitic infection have broad implications for the evolutionary and dynamical impacts of parasites on populations where inbreeding occurs. To rigorously assess the magnitude and the prevalence of inbreeding effects on immunity, multiple components of host immune response should be related to inbreeding coefficient (f) in free-living individuals. We used a pedigreed, free-living population of song sparrows (Melospiza melodia) to test whether individual responses to widely used experimental immune challenges varied consistently with f. The patagial swelling response to phytohaemagglutinin declined markedly with f in both females and males in both 2002 and 2003, although overall inbreeding depression was greater in males. The primary antibody response to tetanus toxoid declined with f in females but not in males in both 2004 and 2005. Primary antibody responses to diphtheria toxoid were low but tended to decline with f in 2004. Overall inbreeding depression did not solely reflect particularly strong immune responses in outbred offspring of immigrant–native pairings or weak responses in highly inbred individuals. These data indicate substantial and apparently sex-specific inbreeding effects on immune response, implying that inbred hosts may be relatively susceptible to parasitic infection to differing degrees in males and females.

Comprehensive paternity assignment: genotype, spatial location and social status in song sparrows, Melospiza Melodia

Comprehensive, accurate paternity assignment is critical to answering numerous questions in evolutionary ecology. Yet, most studies of species with extra‐pair paternity (EPP) fail to assign sires to all offspring. Common limitations include incomplete and biased sampling of offspring and males, particularly with respect to male location and social status, potentially biasing estimated patterns of paternity. Studies that achieve comprehensive sampling and paternity assignment are therefore required. Accordingly, we genotyped virtually all males and >99% of 6‐day‐old offspring over 16 years in a song sparrow (Melospiza melodia) population and used three complementary statistical methodologies to attempt complete paternity assignment for all 2207 offspring. Assignments were highly consistent across maximum likelihood methods that used solely genotype data, and heuristic and integrated Bayesian analyses that included data describing individual locations. Sires were assigned to >99% of all genotyped offspring with ≥95% confidence, revealing an EPP rate of c. 28%. Extra‐pair sires primarily occupied territories neighbouring their extra‐pair offspring; spatial location was therefore highly informative for paternity assignment. EPP was biased towards paired territorial males, although unpaired territorial and floater males sired c. 13% of extra‐pair offspring. Failing to sample and include unpaired males as candidate sires would therefore substantially reduce assignment rates. These analyses demonstrate the integration of genetic and ecological information to achieve comprehensive paternity assignment and direct biological insight, illustrate the potential biases that common forms of incomplete sampling could have on estimated patterns of EPP, and provide an essential basis for understanding the evolutionary causes and consequences of EPP.

Evolution of Mate Choice for Genome-Wide Heterozygosity

The extent to which indirect genetic benefits can drive the evolution of directional mating preferences for more ornamented mates, and the mechanisms that maintain such preferences without depleting genetic variance, remain key questions in evolutionary ecology. We used an individual-based genetic model to examine whether a directional preference for mates with higher genome-wide heterozygosity (H), and consequently greater ornamentation, could evolve and be maintained in the absence of direct fitness benefits of mate choice. We specifically considered finite populations of varying size and spatial genetic structure, in which parent-offspring resemblance in heterozygosity could provide an indirect benefit of mate choice. A directional preference for heterozygous mates evolved under broad conditions, even given a substantial direct cost of mate choice, low mutation rate, and stochastic variation in the link between individual heterozygosity and ornamentation. Furthermore, genetic variance was retained under directional sexual selection. Preference evolution was strongest in smaller populations, but weaker in populations with greater internal genetic structure in which restricted dispersal increased local inbreeding among offspring of neighboring females that all preferentially mated with the same male. These results suggest that directional preferences for heterozygous or outbred mates could evolve and be maintained in finite populations in the absence of direct fitness benefits, suggesting a novel resolution to the lek paradox.

Long-term maternal effect on offspring immune response in song sparrows Melospiza melodia

Knowledge of the causes of variation in host immunity to parasitic infection and the time-scales over which variation persists, is integral to predicting the evolutionary and epidemiological consequences of host–parasite interactions. It is clear that offspring immunity can be influenced by parental immune experience, for example, reflecting transfer of antibodies from mothers to young offspring. However, it is less clear whether such parental effects persist or have functional consequences over longer time-scales, linking a parents previous immune experience to future immune responsiveness in fully grown offspring. We used free-living song sparrows (Melospiza melodia) to quantify long-term effects of parental immune experience on offspring immune response. We experimentally vaccinated parents with a novel antigen and tested whether parental vaccination influenced the humoral antibody response mounted by fully grown offspring hatched the following year. Parental vaccination did not influence offspring baseline antibody titres. However, offspring of vaccinated mothers mounted substantially stronger antibody responses than offspring of unvaccinated mothers. Antibody responses did not differ between offspring of vaccinated and unvaccinated fathers. These data demonstrate substantial long-term effects of maternal immune experience on the humoral immune response of fully grown offspring in free-living birds.

Parent age, lifespan and offspring survival: structured variation in life history in a wild population.

1. Understanding the degree to which reproductive success varies with an individuals age and lifespan, and the degree to which population-level variation mirrors individual-level variation, is central to understanding life-history evolution and the dynamics of age-structured populations. We quantified variation in the survival probability of offspring, one key component of reproductive success and fitness, in relation to parent age and lifespan in a wild population of red-billed choughs (Pyrrhocorax pyrrhocorax). 2. On average across the study population, the first-year survival probability of offspring decreased with increasing parent age and lifespan; offspring of old parents were less likely to survive than offspring of young parents, and offspring of long-lived parents were less likely to survive than offspring of short-lived parents. 3. However, survival did not vary with parent age across offspring produced by groups of parents that ultimately had similar lifespans. 4. Rather, across offspring produced by young parents, offspring survival decreased with increasing parent lifespan; parents that ultimately had long lifespans produced offspring that survived poorly, even when these parents were breeding at young ages. 5. The average decrease in offspring survival with increasing parent age observed across the population therefore reflected the gradual disappearance of short-lived parents that produced offspring that survived well, not age-specific variation in offspring survival within individual parents. 6. The negative correlation between offspring survival and maternal lifespan was strongest when environmental conditions meant that offspring survival was low across the population. 7. These data suggest an environment-dependent trade-off between parent and offspring survival, show consistent individual variation in the resolution of this trade-off that is set early in a parents life, and demonstrate that such structured life-history variation can generate spurious evidence of senescence in key fitness components when measured across a population.

Additive Genetic Variance, Heritability, and Inbreeding Depression in Male Extra-Pair Reproductive Success

The hypothesis that female extra-pair reproduction in socially monogamous animals reflects indirect genetic benefits requires that there be additive and/or nonadditive genetic variance in fitness. However, the specific hypotheses that male extra-pair reproductive success (EPRS) shows additive genetic variance (VA), heritability (h2), or inbreeding depression, and hence that females could acquire indirect genetic benefits through increased EPRS of sons, have not been explicitly tested. We used comprehensive genetic pedigree data from song sparrows (Melospiza melodia) to estimate VA, h2, and inbreeding depression in the number of extra-pair offspring a male sired per year and the probability that a male would sire any extra-pair offspring per year. Inbreeding depression was substantial: more inbred males sired fewer extra-pair offspring and were less likely to sire any extra-pair offspring. In contrast, estimates of VA and h2 were close to 0, although 95% credible intervals were relatively wide. These data suggest that females could accrue indirect genetic benefits, in terms of increased EPRS of outbred sons, by mating with unrelated social or extra-pair mates. In contrast, any indirect benefit of extra-pair reproduction in terms of producing sons with high additive genetic value for EPRS is most likely to be small.