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.

Temporal correlations among demographic parameters are ubiquitous but highly variable across species.

Temporal correlations among demographic parameters can strongly influence population dynamics. Our empirical knowledge, however, is very limited regarding the direction and the magnitude of these correlations and how they vary among demographic parameters and species' life histories. Here, we use long-term demographic data from 15 bird and mammal species with contrasting pace of life to quantify correlation patterns among five key demographic parameters: juvenile and adult survival, reproductive probability, reproductive success and productivity. Correlations among demographic parameters were ubiquitous, more frequently positive than negative, but strongly differed across species. Correlations did not markedly change along the slow-fast continuum of life histories, suggesting that they were more strongly driven by ecological than evolutionary factors. As positive temporal demographic correlations decrease the mean of the long-run population growth rate, the common practice of ignoring temporal correlations in population models could lead to the underestimation of extinction risks in most species.

Divorce in an Island Bird Population: Causes, Consequences, and Lack of Inheritance.

Divorce (mate switching) is widely considered an adaptive strategy that female birds use to improve their reproductive success. However, in few species are the causes and consequences of divorce well understood, and the genetic basis and inheritance of divorce have never been explored. In Savannah sparrows (Passerculus sandwichensis) breeding on Kent Island, New Brunswick, Canada, 47.0% of pairs in which both partners survived to the following breeding season ended in divorce. Secondary females, which received less parental assistance than primary females, tended to divorce when breeding success was low or when paired with small males. Unlike young females or widows, older females improved their fledging success after divorce. Young males (but not older males) suffered lower reproductive success following a divorce. However, neither the lifetime number of divorces nor whether an individual had ever divorced affected the fitness of females or males, which suggests little or no selection for the trait. We found moderate repeatability for divorce in females (although not in males) but no additive genetic variance or evidence of maternal or paternal effects. Divorce in Savannah sparrows appears to be a nonheritable flexible behavior whose expression and consequences depend on an individual's sex, mating status, size, and age.

Local density regulates migratory songbird reproductive success through effects on double-brooding and nest predation.

Knowledge of the density-dependent processes that regulate animal populations is key to understanding, predicting, and conserving populations. In migratory birds, density-dependence is most often studied during the breeding season, yet we still lack a robust understanding of the reproductive traits through which density influences individual reproductive success. We used 27-yr of detailed, individual-level productivity data from an island-breeding population of Savannah sparrows Passerculus sandwichensis to evaluate effects of local and total annual population density on female reproductive success. Local density (number of neighbors within 50 m of a female's nest) had stronger effects on the number of young fledged than did total annual population density. Females nesting in areas of high local density were more likely to suffer nest predation and less likely to initiate and fledge a second clutch, which led to fewer young fledged in a season. Fledging fewer young subsequently decreased the likelihood of a female recruiting offspring into the breeding population in a subsequent year. Collectively, these results provide insight into the scale and reproductive mechanisms mediating density-dependent reproductive success and fitness in songbirds.

Differential migration and the link between winter latitude, timing of migration, and breeding in a songbird.

Patterns of connectivity between breeding and wintering grounds can have important implications for individual fitness and population dynamics. Using light-level geolocators and stable hydrogen isotopes (δ(2)H) in feathers, we evaluated differential migration of Savannah sparrows (Passerculus sandwichensis) breeding on Kent Island in the Bay of Fundy, New Brunswick, Canada in relation to sex, age, and body size. Based on geolocators recovered from 38 individuals between 2012 and 2014, the winter distribution was centered in North Carolina (median latitude 34°, range 26°-41°), with males overwintering, on average, approximately 275 km further north than females. Based on analyses of tail feather samples collected from 106 individuals from the same population between 2008 and 2012, males and adults had more negative δ(2)H values than females and juveniles, respectively, providing additional evidence that males wintered north of females and that adults wintered north of juveniles. Winter latitude and δ(2)H values within each sex were not found to be related to body size. From geolocator data, males returned to the breeding grounds, on average, 14 days earlier than females. For males, there was some evidence that arrival date on the breeding grounds was negatively correlated with winter latitude and that individuals which arrived earlier tended to breed earlier. Thus, benefits for males of early arrival on the breeding grounds may have contributed to their wintering farther north than females. Social dominance may also have contributed to age and sex differences in winter latitude, whereby dominant males and adults forced subordinate females and juveniles further south.

Leaf size in three generations of a dioecious tropical tree, Ocotea tenera (Lauraceae): Sexual dimorphism and changes with age.

PREMISE OF THE STUDY: In dioecious species, selection should favor different leaf sizes in males and females whenever the sexes experience distinct environments or constraints such as different costs of reproduction. We took advantage of a long-term experimental study of Ocotea tenera (Lauraceae), a dioecious understory tree in Monteverde, Costa Rica, to explore leaf size differences between genders and age classes across generations. METHODS: We measured leaf size in adult trees in a natural population, in their adult F(1) offspring in two experimental populations, and in their F(2) offspring at the seedling stage. Individual trees were measured at various times over 20 yr. RESULTS: Leaves of female trees averaged 8% longer and 12% greater in area than those of males. Leaves were sexually dimorphic at reproductive maturity. Leaf size declined during the lifetime of most trees. Heritability estimates for leaf length were positive although not statistically significant (h(2) = 0.63, SE = 0.48, P = 0.095). CONCLUSIONS: We ruled out the ecological causation hypothesis for sexual dimorphism in leaf size because male and female trees co-occurred in the same habitats. Sexual dimorphism appeared not to result from genetic or phenotypic correlations with other traits such as height or flower size. Rather, females appear to compensate for higher costs of reproduction and diminished photosynthetic capacity by producing larger leaves. Additive genetic variance in leaf size, a prerequisite for an evolutionary response to selection for sexual dimorphism, was suggested by positive (although only marginally significant) heritability estimates.

Natal experience and pre-breeding environmental conditions affect lay date plasticity in Savannah Sparrows.

Phenotypic plasticity allows organisms to adjust the timing of life-history events in response to environmental and demographic conditions. Shifts by individuals in the timing of breeding with respect to variation in age and temperature are well documented in nature, and these changes are known to scale to affect population dynamics. However, relatively little is known about how organisms alter phenology in response to other demographic and environmental factors. We investigated how pre-breeding temperature, breeding population density, age, and rainfall in the first month of life influenced the timing and plasticity of lay date in a population of Savannah Sparrows (Passerculus sandwichensis) monitored over 33 yr (1987-2019). Females that experienced warmer pre-breeding temperatures tended to lay eggs earlier, as did older females, but breeding population density had no effect on lay date. Natal precipitation interacted with age to influence lay date plasticity, with females that experienced high precipitation levels as nestlings advancing lay dates more strongly over the course of their lives. We also found evidence for varied pace of life; females that experienced high natal precipitation had shorter lifespans and reduced fecundity, but more nesting attempts over their lifetimes. Rainfall during the nestling period increased through time, while population density and fecundity declined, suggesting that increased precipitation on the breeding grounds may be detrimental to breeding females and ultimately the viability of the population as a whole. Our results suggest that females adjust their laying date in response to pre-breeding temperature, and as they age, while presenting new evidence that environmental conditions during the natal period can affect phenological plasticity and generate downstream, population-level effects.

The rate of telomere loss is related to maximum lifespan in birds.

Telomeres are highly conserved regions of DNA that protect the ends of linear chromosomes. The loss of telomeres can signal an irreversible change to a cell's state, including cellular senescence. Senescent cells no longer divide and can damage nearby healthy cells, thus potentially placing them at the crossroads of cancer and ageing. While the epidemiology, cellular and molecular biology of telomeres are well studied, a newer field exploring telomere biology in the context of ecology and evolution is just emerging. With work to date focusing on how telomere shortening relates to individual mortality, less is known about how telomeres relate to ageing rates across species. Here, we investigated telomere length in cross-sectional samples from 19 bird species to determine how rates of telomere loss relate to interspecific variation in maximum lifespan. We found that bird species with longer lifespans lose fewer telomeric repeats each year compared with species with shorter lifespans. In addition, phylogenetic analysis revealed that the rate of telomere loss is evolutionarily conserved within bird families. This suggests that the physiological causes of telomere shortening, or the ability to maintain telomeres, are features that may be responsible for, or co-evolved with, different lifespans observed across species.This article is part of the theme issue 'Understanding diversity in telomere dynamics'.

Winter temperatures limit population growth rate of a migratory songbird.

Understanding the factors that limit and regulate wildlife populations requires insight into demographic and environmental processes acting throughout the annual cycle. Here, we combine multi-year tracking data of individual birds with a 26-year demographic study of a migratory songbird to evaluate the relative effects of density and weather at the breeding and wintering grounds on population growth rate. Our results reveal clear support for opposing forces of winter temperature and breeding density driving population dynamics. Above-average temperatures at the wintering grounds lead to higher population growth, primarily through their strong positive effects on survival. However, population growth is regulated over the long term by strong negative effects of breeding density on both fecundity and adult male survival. Such knowledge of how year-round factors influence population growth, and the demographic mechanisms through which they act, will vastly improve our ability to predict species responses to environmental change and develop effective conservation strategies for migratory animals.

Little effect of extrapair paternity on the opportunity for sexual selection in Savannah sparrows (Passerculus sandwichensis).

Extrapair paternity (EPP) can dramatically increase the opportunity for sexual selection if relatively few males are able to monopolize the majority of fertilizations in a population. Although recent work with birds suggests that EPP can increase the standardized variance in male reproductive success (Is) as much as 13-fold, only a male's within-pair success is typically quantified with any accuracy. In most cases, nearly half of all extrapair young are of unknown parentage. A strong, negative correlation across studies between the proportion of extrapair young for which parentage is known and the apparent effect of EPP on Is (r(s) = -0.71, P = 0.013, N = 13 studies) suggests that the incomplete sampling of extrapair sires has greatly exaggerated the influence of EPP. To achieve a more thorough accounting of EPP and its importance to variation in male fitness, we used a suite of four to six microsatellite loci to identify extrapair young and their sires in a polygynous population of Savannah sparrows (Passerculus sandwichensis). Pooling over the 2002 and 2003 breeding seasons, 79 of 116 females (68.1%) produced young outside of the pairbond and 194 of 411 offspring (47.2%) were extrapair. We identified sires for 96.4% of all young (N = 396), including sires for 92.3% of the extrapair young (N = 179), allowing us to partition Is into within-pair and extrapair components. In both years, EPP-related fitness components generated more variation in male reproductive success than the number or quality of within-pair mates. Differences among males in the number of extrapair mates alone accounted for 56.6% of Is in 2002 and for 23.6% of Is in 2003. Nonetheless, in absolute terms, the occurrence of EPP on Kent Island increased the opportunity for sexual selection less than two-fold. Averaging over the two years, Is was only 78% higher than Is,app, the variance in male reproductive success that would have occurred had EPP been nonexistent and males sired all young on their territories. Likewise, across nine socially monogamous species, we found no correlation between the extent of EPP and its effect on the opportunity for sexual selection (Is/Is,app) and only a marginally significant positive correlation between EPP and Is itself. Taken together, our results suggest that the relationship between EPP and sexual selection in birds may be much less strong and much less straightforward than commonly thought.

Genetic structure in a population of a tropical tree Ocotea tenera (Lauraceae): influence of avian seed dispersal.

We studied the influence of avian seed dispersal on the structuring of genetic diversity in a population of a tropical tree, Ocotea tenera (Lauraceae). The seeds of O. tenera are principally dispersed by four, relatively specialized, fruit-eating bird species (emerald toucanets, keel-billed toucans, resplendent quetzals, and three-wattled bellbirds). We found high genetic diversity within the overall population and significant, nonrandom structuring of that diversity among subpopulations. Subpopulations contained members of several sibling groups, and most saplings within subpopulations were shown not to be the progeny of adult trees within the same subpopulation. Our data indicate that O. tenera subpopulations are founded with several seeds from few maternal families, and that this mode of establishment is an important determinant of population genetic architecture.

The effect of trait type and strength of selection on heritability and evolvability in an island bird population.

The heritability (h(2) ) of fitness traits is often low. Although this has been attributed to directional selection having eroded genetic variation in direct proportion to the strength of selection, heritability does not necessarily reflect a trait's additive genetic variance and evolutionary potential ("evolvability"). Recent studies suggest that the low h(2) of fitness traits in wild populations is caused not by a paucity of additive genetic variance (VA ) but by greater environmental or nonadditive genetic variance (VR ). We examined the relationship between h(2) and variance-standardized selection intensities (i or ßσ ), and between evolvability (IA :VA divided by squared phenotypic trait mean) and mean-standardized selection gradients (ßµ ). Using 24 years of data from an island population of Savannah sparrows, we show that, across diverse traits, h(2) declines with the strength of selection, whereas IA and IR (VR divided by squared trait mean) are independent of the strength of selection. Within trait types (morphological, reproductive, life-history), h(2) , IA , and IR are all independent of the strength of selection. This indicates that certain traits have low heritability because of increased residual variance due to the age at which they are expressed or the multiple factors influencing their expression, rather than their association with fitness.

Assessing multivariate constraints to evolution across ten long-term avian studies.

BACKGROUND: In a rapidly changing world, it is of fundamental importance to understand processes constraining or facilitating adaptation through microevolution. As different traits of an organism covary, genetic correlations are expected to affect evolutionary trajectories. However, only limited empirical data are available. METHODOLOGY/PRINCIPAL FINDINGS: We investigate the extent to which multivariate constraints affect the rate of adaptation, focusing on four morphological traits often shown to harbour large amounts of genetic variance and considered to be subject to limited evolutionary constraints. Our data set includes unique long-term data for seven bird species and a total of 10 populations. We estimate population-specific matrices of genetic correlations and multivariate selection coefficients to predict evolutionary responses to selection. Using Bayesian methods that facilitate the propagation of errors in estimates, we compare (1) the rate of adaptation based on predicted response to selection when including genetic correlations with predictions from models where these genetic correlations were set to zero and (2) the multivariate evolvability in the direction of current selection to the average evolvability in random directions of the phenotypic space. We show that genetic correlations on average decrease the predicted rate of adaptation by 28%. Multivariate evolvability in the direction of current selection was systematically lower than average evolvability in random directions of space. These significant reductions in the rate of adaptation and reduced evolvability were due to a general nonalignment of selection and genetic variance, notably orthogonality of directional selection with the size axis along which most (60%) of the genetic variance is found. CONCLUSIONS: These results suggest that genetic correlations can impose significant constraints on the evolution of avian morphology in wild populations. This could have important impacts on evolutionary dynamics and hence population persistence in the face of rapid environmental change.

Early life events carry over to influence pre-migratory condition in a free-living songbird.

Conditions experienced during development can have long-term consequences for individual success. In migratory songbirds, the proximate mechanisms linking early life events and survival are not well understood because tracking individuals across stages of the annual cycle can be extremely challenging. In this paper, we first use a 13 year dataset to demonstrate a positive relationship between 1(st) year survival and nestling mass in migratory Savannah sparrows (Passerculus sandwichensis). We also use a brood manipulation experiment to show that nestlings from smaller broods have higher mass in the nest relative to individuals from larger broods. Having established these relationships, we then use three years of field data involving multiple captures of individuals throughout the pre-migratory period and a multi-level path model to examine the hypothesis that conditions during development limit survival during migration by affecting an individual's ability to accumulate sufficient lean tissue and fat mass prior to migration. We found a positive relationship between fat mass during the pre-migratory period (Sept-Oct) and nestling mass and a negative indirect relationship between pre-migratory fat mass and fledging date. Our results provide the first evidence that conditions during development limit survival during migration through their effect on fat stores. These results are particularly important given recent evidence showing that body condition of songbirds at fledging is affected by climate change and anthropogenic changes to landscape structure.

Previous-year reproduction reduces photosynthetic capacity and slows lifetime growth in females of a neotropical tree.

Females of dioecious plant species typically invest more in reproduction than males because they produce seeds, fruits, and associated structures in addition to flowers. If females are unable to compensate by up-regulating rates of photosynthesis or by reproducing less frequently than males, their greater reproductive investment may result in reduced growth or higher mortality. Here we provide evidence of the cost of reproduction in Ocotea tenera (Lauraceae), a dioecious neotropical tree common in lower montane forests of Monteverde, Costa Rica. Over periods of 12-21 years, females grew more slowly than males in a natural population and in two experimental plots where we were able to control for genotype, age, habitat, and reproductive history. Simultaneous measurements of 10 matched pairs of sibling trees of the opposite sex but same age demonstrated that the photosynthetic capacities of females were 13% lower than those of males. Among females, photosynthetic capacity was negatively correlated with fruit production during the most recent reproductive season but not with lifetime fruit production. Sexual size dimorphism in adult O. tenera trees appears to be a nonadaptive consequence of trading off recent reproduction against maintenance of the photosynthetic apparatus, with long-term negative effects on growth.

Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird.

Female birds often copulate outside the pair-bond to produce broods of mixed paternity, but despite much recent attention the adaptive significance of this behaviour remains elusive. Although several studies support the idea that extra-pair copulations (EPCs) allow females to obtain 'good genes' for their offspring, many others have found no relationship between female mating fidelity and traits likely to reflect male quality. A corollary to the good genes hypothesis proposes that females do use EPCs to increase the quality of young, but it is the interaction between maternal and paternal genomes - and not male quality per se - that is the target of female choice. We tested this 'genetic compatibility' hypothesis in a free-living population of Savannah sparrows (Passerculus sandwichensis) by determining whether females mated nonrandomly with respect to the major histocompatibility complex (Mhc). During both the 1994 and 1995 breeding seasons, female yearlings (but not older birds) avoided pairing with Mhc-similar males (P < 0.005). The Mhc similarity between mates also predicted the occurrence of extra-pair young in first broods (P < 0.007) and covaried with estimates of genome-wide levels of similarity derived from multilocus DNA fingerprinting profiles (P = 0.007). The overall genetic similarity between adults tended to predict female mating fidelity, but with less precision than their Mhc similarity (P = 0.09). In contrast, females appeared insensitive to the size, weight or age of males, none of which explained variation in female mating fidelity. Taken together, these results are consistent with the hypothesis that females sought complementary genes for their offspring and suggest either that the benefits of heterozygosity (at the Mhc) drive female mating patterns or that the avoidance of inbreeding is an ultimate cause of social and genetic mate choice in Savannah sparrows.