Fluctuating optimum and temporally variable selection on breeding date in birds and mammals

International audienceTemporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection

Inbreeding is associated with shorter early-life telomere length in a wild passerine

Abstract Inbreeding can have negative effects on survival and reproduction, which may be of conservation concern in small and isolated populations. However, the physiological mechanisms underlying inbreeding depression are not well-known. The length of telomeres, the DNA sequences protecting chromosome ends, has been associated with health or fitness in several species. We investigated effects of inbreeding on early-life telomere length in two small island populations of wild house sparrows (Passer domesticus) known to be affected by inbreeding depression. Using genomic measures of inbreeding we found that inbred nestling house sparrows (n = 371) have significantly shorter telomeres. Using pedigree-based estimates of inbreeding we found a tendency for inbred nestling house sparrows to have shorter telomeres (n = 1195). This negative effect of inbreeding on telomere length may have been complemented by a heterosis effect resulting in longer telomeres in individuals that were less inbred than the population average. Furthermore, we found some evidence of stronger effects of inbreeding on telomere length in males than females. Thus, telomere length may reveal subtle costs of inbreeding in the wild and demonstrate a route by which inbreeding negatively impacts the physiological state of an organism already at early life-history stages

Resistance to gapeworm parasite has both additive and dominant genetic components in house sparrows, with evolutionary consequences for ability to respond to parasite challenge

Abstract Host–parasite relationships are likely to change over the coming decades in response to climate change and increased anthropogenic stressors. Understanding the genetic architecture of parasite resistance will aid prediction of species’ responses to intensified parasite challenge. The gapeworm “Syngamus trachea” is prevalent in natural bird populations and causes symptomatic infections ranging from mild to severe. The parasite may affect ecological processes by curtailing bird populations and is important due to its propensity to spread to commercially farmed birds. Our large‐scale data set on an insular house sparrow metapopulation in northern Norway includes information on gapeworm prevalence and infection intensity, allowing assessment of the genetics of parasite resistance in a natural system. To determine whether parasite resistance has a heritable genetic component, we performed variance component analyses using animal models. Resistance to gapeworm had substantial additive genetic and dominance variance, and genome‐wide association studies to identify single nucleotide polymorphisms associated with gapeworm resistance yielded multiple loci linked to immune function. Together with genome partitioning results, this indicates that resistance to gapeworm is under polygenic control in the house sparrow, and probably in other bird species. Hence, our results provide the foundation needed to study any eco‐evolutionary processes related to gapeworm infection, and show that it is necessary to use methods suitable for polygenic and nonadditive genetic effects on the phenotype

Variation in generation time reveals density regulation as an important driver of pace of life in a bird metapopulation

Abstract Generation time determines the pace of key demographic and evolutionary processes. Quantified as the weighted mean age at reproduction, it can be studied as a life-history trait that varies within and among populations and may evolve in response to ecological conditions. We combined quantitative genetic analyses with age- and density-dependent models to study generation time variation in a bird metapopulation. Generation time was heritable, and males had longer generation times than females. Individuals with longer generation times had greater lifetime reproductive success but not a higher expected population growth rate. Density regulation acted on recruit production, suggesting that longer generation times should be favoured when populations are closer to carrying capacity. Furthermore, generation times were shorter when populations were growing and longer when populations were closer to equilibrium or declining. These results support classic theory predicting that density regulation is an important driver of the pace of life-history strategies

Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation

Abstract Inbreeding may increase the extinction risk of small populations. Yet, studies using modern genomic tools to investigate inbreeding depression in nature have been limited to single populations, and little is known about the dynamics of inbreeding depression in subdivided populations over time. Natural populations often experience different environmental conditions and differ in demographic history and genetic composition, characteristics that can affect the severity of inbreeding depression. We utilized extensive long-term data on more than 3,100 individuals from eight islands in an insular house sparrow metapopulation to examine the generality of inbreeding effects. Using genomic estimates of realized inbreeding, we discovered that inbred individuals had lower survival probabilities and produced fewer recruiting offspring than noninbred individuals. Inbreeding depression, measured as the decline in fitness-related traits per unit inbreeding, did not vary appreciably among populations or with time. As a consequence, populations with more resident inbreeding (due to their demographic history) paid a higher total fitness cost, evidenced by a larger variance in fitness explained by inbreeding within these populations. Our results are in contrast to the idea that effects of inbreeding generally depend on ecological factors and genetic differences among populations, and expand the understanding of inbreeding depression in natural subdivided populations