Variation in movement strategies: Capital versus income migration.

Animal migrations represent the regular movements of trillions of individuals. The scale of these movements has inspired human intrigue for millennia and has been intensively studied by biologists. This research has highlighted the diversity of migratory strategies seen across and within migratory taxa: while some migrants temporarily express phenotypes dedicated to travel, others show little or no phenotypic flexibility in association with migration. However, a vocabulary for describing these contrasting solutions to the performance trade-offs inherent to the highly dynamic lifestyle of migrants (and strategies intermediate between these two extremes) is currently missing. We propose a taxon-independent organising framework based on energetics, distinguishing between migrants that forage as they travel (income migrants) and those that fuel migration using energy acquired before departure (capital migrants). Not only does our capital:income continuum of migratory energetics account for the variable extent of phenotypic flexibility within and across migrant populations, but it also aligns with theoreticians' treatment of migration and clarifies how migration impacts other phases of the life cycle. As such, it provides a unifying scale and common vacabulary for comparing the migratory strategies of divergent taxa.

Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals.

The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.

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

Temporal 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.

It takes two: Heritable male effects on reproductive timing but not clutch size in a wild bird population.

Within-population variation in the traits underpinning reproductive output has long been of central interest to biologists. Since they are strongly linked to lifetime reproductive success, these traits are expected to be subject to strong selection and, if heritable, to evolve. Despite the formation of durable pair bonds in many animal taxa, reproductive traits are often regarded as female-specific, and estimates of quantitative genetic variation seldom consider a potential role for heritable male effects. Yet reliable estimates of such social genetic effects are important since they influence the amount of heritable variation available to selection. Based on a 52-year study of a nestbox-breeding great tit (Parus major) population, we apply "extended" bivariate animal models in which the heritable effects of both sexes are modeled to assess the extent to which males contribute to heritable variation in seasonal reproductive timing (egg laying date) and clutch size, while accommodating the covariance between the two traits. Our analyses show that reproductive timing is a jointly expressed trait in this species, with (positively covarying) heritable variation for laydate being expressed in both members of a breeding pair, such that the total heritable variance is 50% larger than estimated by traditional models. This result was robust to explicit consideration of a potential male-biased environmental confound arising through sexually dimorphic dispersal. In contrast to laydate, males' contribution to heritable variation in clutch size was limited. Our study thus highlights the contrasting extent of social determination for two major components of annual reproductive success, and emphasizes the need to consider the social context of what are often considered individual-level traits.

Accounting for interspecific competition and age structure in demographic analyses of density dependence improves predictions of fluctuations in population size.

Understanding species coexistence has long been a major goal of ecology. Coexistence theory for two competing species posits that intraspecific density dependence should be stronger than interspecific density dependence. Great tits and blue tits are two bird species that compete for food resources and nesting cavities. On the basis of long-term monitoring of these two competing species at sites across Europe, combining observational and manipulative approaches, we show that the strength of density regulation is similar for both species, and that individuals have contrasting abilities to compete depending on their age. For great tits, density regulation is driven mainly by intraspecific competition. In contrast, for blue tits, interspecific competition contributes as much as intraspecific competition, consistent with asymmetric competition between the two species. In addition, including age-specific effects of intra- and interspecific competition in density-dependence models improves predictions of fluctuations in population size by up to three times.

Heritable spouse effects increase evolutionary potential of human reproductive timing.

Sexual reproduction is inherently interactive, especially in animal species such as humans that exhibit extended pair bonding. Yet we have little knowledge of the role of male characteristics and their evolutionary impact on reproductive behavioural phenotypes, to the extent that biologists typically consider component traits (e.g. reproductive timing) as female-specific. Based on extensive genealogical data detailing the life histories of 6435 human mothers born across four centuries of modern history, we use an animal modelling approach to estimate the indirect genetic effect of men on the reproductive phenotype of their partners. These analyses show that a woman's reproductive timing (age at first birth) is influenced by her partner's genotype. This indirect genetic effect is positively correlated with the direct genetic effect expressed in women, such that total heritable variance in this trait is doubled when heritable partner effects are considered. Our study thus suggests that much of the heritable variation in women's reproductive timing is mediated via partner effects, and that the evolutionary potential of this trait is far greater than previously appreciated.

Climate change upends selection on ornamentation in a wild bird.

Secondary sexual traits have high heritabilities and are exposed to strong, environmentally sensitive selection, and so are expected to evolve rapidly in response to sustained environmental change. We examine the eco-evolutionary dynamics of ornament expression in a long-term study population of collared flycatchers, Ficedula albicollis, in which forehead patch size, which positively influences male reproductive success, declined markedly over 34 years. Annual fitness selection on forehead patch size switched from positive to negative during the study, a reversal that is accounted for by rising spring temperatures at the breeding site: highly ornamented males were selectively favoured following cold breeding seasons but selected against following warm breeding seasons. An 'individual animal model' describes a decline in the genetic values of breeding males during the study, which simulations showed was unlikely to result from drift alone. These results are thus consistent with adaptive evolution of a sexually selected trait in response to climate change.

Nonautosomal genetic variation in carotenoid coloration.

Carotenoid-based coloration plays an important role in signaling, is often sexually dimorphic, and is potentially subject to directional and/or sex-specific selection. To understand the evolutionary dynamics of such color traits, it is essential to quantify patterns of inheritance, yet nonautosomal sources of genetic variation are easily overlooked by classical heritability analyses. Carotenoid metabolism has recently been linked to mitochondria, highlighting the potential for color variation to be explained by cytoplasmically inherited factors. In this study, we used quantitative genetic animal models to estimate the importance of mitochondrial and sex chromosome-linked sources of genetic variation in coloration in two songbird populations in which dietary carotenoids are either unmodified (great tit plumage) or metabolized into alternative color forms (zebra finch beak). We found no significant Z-linked genetic variance in great tit plumage coloration, while zebra finch beak coloration exhibited significant W linkage and cytoplasmic inheritance. Our results support cytoplasmic inheritance of color in the zebra finch, a trait based on endogenously metabolized carotenoids, and demonstrate the potential for nonautosomal sources to account for a considerable share of genetic variation in coloration. Although often overlooked, such nonautosomal genetic variation exhibits sex-dependent patterns of inheritance and potentially influences the evolution of sexual dichromatism.

Pigments versus structure: examining the mechanism of age-dependent change in a carotenoid-based colour.

Within-population colour variation is widespread in animals, yet the determinants of variable coloration have been relatively neglected by ecologists. Age-dependent expression of conspicuous coloration is prevalent, particularly in birds. Such patterns can be generated by multiple combinations of demographic heterogeneity or within-individual change; longitudinal analyses are necessary to establish the importance of these processes. Further, although pigment-based colours are composite traits, produced by multiple component mechanisms (e.g. feather microstructure and carotenoid pigmentation), the contributions of these mechanisms to components of age dependence are rarely considered, even though doing so may yield information about the ecological causes for age-dependent coloration. We used a large-scale, longitudinal study of carotenoid-based plumage coloration in great tits (Parus major) to show age dependence of plumage coloration is driven almost exclusively by within-individual effects in the first 2 years of life. Using wavelength-specific analyses, we show that feather microstructure, while sensitive to annual variation, is independent of age, with increased carotenoid deposition driving changes in coloration. However, estimates of local carotenoid availability did not explain the change in coloration within individuals, suggesting that pigment availability may not be limiting. We thus show that it is individual-level changes in the pigment component of carotenoid-based coloration that determines age-dependent colour expression in great tits. More generally, our study highlights the utility of wavelength-specific analyses in determining the mechanisms underlying changes in expression of composite colour traits.

Quantitative genetics of a carotenoid-based color: heritability and persistent natal environmental effects in the great tit.

The information content of signals such as animal coloration depends on the extent to which variation reflects underlying biological processes. Although animal coloration has received considerable attention, little work has addressed the quantitative genetics of color variation in natural populations. We investigated the quantitative genetics of a carotenoid-based color patch, the ventral plumage of mature great tits (Parus major), in a wild population. Carotenoid-based colors are often suggested to reflect environmental variation in carotenoid availability, but numerous mechanisms could also lead to genetic variation in coloration. Analyses of individuals of known origin showed that, although plumage chromaticity (i.e., color) was moderately heritable, there was no significant heritability to achromaticity (i.e., brightness). We detected multiple long-lasting effects of natal environment, with hatching date and brood size both negatively related to plumage chromaticity at maturity. Our reflectance measures contrasted in their spatiotemporal sensitivity, with plumage chromaticity exhibiting significant spatial variation and achromatic variation exhibiting marked annual variation. Hence, color variation in this species reflects both genetic and environmental influences on different scales. Our analyses demonstrate the context dependence of components of color variation and suggest that color patches may convey multiple aspects of individual state.

Divergent patterns of age-dependence in ornamental and reproductive traits in the collared flycatcher.

Sexual ornaments are predicted to honestly signal individual condition. We might therefore expect ornament expression to show a senescent decline, in parallel with late-life deterioration of other characters. Conversely, life-history theory predicts the reduced residual reproductive value of older individuals will favor increased investment in sexually attractive traits. Using a 25-year dataset of more than 5000 records of breeding collared flycatchers (Ficedula albicollis) of known age, we quantify cross-sectional patterns of age-dependence in ornamental plumage traits and report long-term declines in expression that mask highly significant positive age-dependency. We partition this population-level age-dependency into its between- and within-individual components and show expression of ornamental white plumage patches exhibits within-individual increases with age in both sexes, consistent with life-history theory. For males, ornament expression also covaries with life span, such that, within a cohort, ornamentation indicates survival. Finally, we compared longitudinal age-dependency of reproductive traits and ornamental traits in both sexes, to assess whether these two trait types exhibit similar age-dependency. These analyses revealed contrasting patterns: reproductive traits showed within-individual declines in late-life females consistent with senescence; ornamental traits showed the opposite pattern in both males and females. Hence, our results for both sexes suggest that age-dependent ornament expression is consistent with life-history models of optimal signaling and, unlike reproductive traits, proof against senescence.

Interspecific patterns of genetic diversity in birds: correlations with extinction risk.

Birds are frequently used as indicators of ecosystem health and are the most comprehensively studied class in the animal kingdom. Nevertheless, a comprehensive, interspecific assessment of the correlates of avian genetic diversity is lacking, even though indices of genetic diversity are of considerable interest in the conservation of threatened species. We used published data on variation at microsatellite loci from 194 bird species to examine correlates of diversity, particularly with respect to conservation status and population size. We found a significant decline in mean heterozygosity with increasing extinction risk, and showed, by excluding species whose heterozygosity values were calculated with heterospecific primers, that this relationship was not dependent on ascertainment bias. Results of subsequent regression analyses suggested that smaller population sizes of threatened species were largely responsible for this relationship. Thus, bird species at risk of extinction are relatively depauperate in terms of neutral genetic diversity, which is expected to make population recovery more difficult if it reflects adaptive genetic variation. Conservation policy will need to minimize further loss of diversity if the chances of saving threatened species are to be maximized.