Climate-mediated population dynamics of a migratory songbird differ between the trailing edge and range core.

Understanding the demographic drivers of range contractions is important for predicting species' responses to climate change; however, few studies have examined the effects of climate change on survival and recruitment across species' ranges. We show that climate change can drive trailing edge range contractions through the effects on apparent survival, and potentially recruitment, in a migratory songbird. We assessed the demographic drivers of trailing edge range contractions using a long-term demography dataset for the black-throated blue warbler (Setophaga caerulescens) collected across elevational climate gradients at the trailing edge and core of the breeding range. We used a Bayesian hierarchical model to estimate the effect of climate change on apparent survival and recruitment and to forecast population viability at study plots through 2040. The trailing edge population at the low-elevation plot became locally extinct by 2017. The local population at the mid-elevation plot at the trailing edge gradually declined and is predicted to become extirpated by 2040. Population declines were associated with warming temperatures at the mid-elevation plot, although results were more equivocal at the low-elevation plot where we had fewer years of data. Population density was stable or increasing at the range core, although warming temperatures are predicted to cause population declines by 2040 at the low-elevation plot. This result suggests that even populations within the geographic core of the range are vulnerable to climate change. The demographic drivers of local population declines varied between study plots, but warming temperatures were frequently associated with declining rates of population growth and apparent survival. Declining apparent survival in our study system is likely to be associated with increased adult emigration away from poor-quality habitats. Our results suggest that demographic responses to warming temperatures are complex and dependent on local conditions and geographic range position, but spatial variation in population declines is consistent with the climate-mediated range shift hypothesis. Local populations of black-throated blue warblers near the warm-edge range boundary at low latitudes and low elevations are likely to be the most vulnerable to climate change, potentially leading to local extirpation and range contractions.

Artificial light at night increases top-down pressure on caterpillars: experimental evidence from a light-naive forest.

Artificial light at night (ALAN) is a globally widespread and expanding form of anthropogenic change that impacts arthropod biodiversity. ALAN alters interspecific interactions between arthropods, including predation and parasitism. Despite their ecological importance as prey and hosts, the impact of ALAN on larval arthropod stages, such as caterpillars, is poorly understood. We examined the hypothesis that ALAN increases top-down pressure on caterpillars from arthropod predators and parasitoids. We experimentally illuminated study plots with moderate levels (10-15 lux) of LED lighting at light-naive Hubbard Brook Experimental Forest, New Hampshire. We measured and compared between experimental and control plots: (i) predation on clay caterpillars, and (ii) abundance of arthropod predators and parasitoids. We found that predation rates on clay caterpillars and abundance of arthropod predators and parasitoids were significantly higher on ALAN treatment plots relative to control plots. These results suggest that moderate levels of ALAN increase top-down pressure on caterpillars. We did not test mechanisms, but sampling data indicates that increased abundance of predators near lights may play a role. This study highlights the importance of examining the effects of ALAN on both adult and larval life stages and suggests potential consequences of ALAN on arthropod populations and communities.

Variance in within-pair reproductive success influences the opportunity for selection annually and over the lifetimes of males in a multibrooded songbird.

In socially monogamous species, male reproductive success consists of "within-pair" offspring produced with their socially paired mate(s), and "extra-pair" offspring produced with additional females throughout the population. Both reproductive pathways offer distinct opportunities for selection in wild populations, as each is composed of separate components of mate attraction, female fecundity, and paternity allocation. Identifying key sources of variance and covariance among these components is a crucial step toward understanding the reproductive strategies that males use to maximize fitness both annually and over their lifetimes. We use 16 years of complete reproductive data from a population of black-throated blue warblers (Setophaga caerulescens) to partition variance in male annual and lifetime reproductive success, and thereby identify if the opportunity for selection varies over the lifetimes of individual males and what reproductive strategies likely favor maximum lifetime fitness. The majority of variance in male reproduction was attributable to within-pair success, but the specific effects of individual components of variance differed between total annual and total lifetime reproductive success. Positive overall lifetime covariance between within-pair and extra-pair components indicates that males able to maximize within-pair success, particularly with double-brooding females, likely achieve higher overall lifetime fitness via both within-pair and extra-pair reproductive pathways.

Common Field Data Limitations Can Substantially Bias Sexual Selection Metrics.

Sexual selection studies widely estimate several metrics, but values may be inaccurate because standard field methods for studying wild populations produce limited data (e.g., incomplete sampling, inability to observe copulations directly). We compared four selection metrics (Bateman gradient, opportunity for sexual selection, opportunity for selection, and smax') estimated with simulated complete and simulated limited data for 15 socially monogamous songbird species with extrapair paternity (4%-54% extrapair offspring). Inferring copulation success from offspring parentage creates nonindependence between these variables and systematically underestimates copulation success. We found that this introduces substantial bias for the Bateman gradient, opportunity for sexual selection, and smax'. Notably, 47.5% of detected Bateman gradients were significantly positive for females, suggesting selection on females to copulate with multiple males, although the true Bateman gradient was zero. Bias generally increased with the extent of other sources of data limitations tested (nest predation, male infertility, and unsampled floater males). Incomplete offspring sampling introduced bias for all of the metrics except the Bateman gradient, while incomplete sampling of extrapair sires did not introduce additional bias when sires were a random subset of breeding males. Overall, our findings demonstrate how biases due to field data limitations can strongly impact the study of sexual selection.

Ecological and Social Factors Constrain Spatial and Temporal Opportunities for Mating in a Migratory Songbird.

Many studies of sexual selection assume that individuals have equal mating opportunities and that differences in mating success result from variation in sexual traits. However, the inability of sexual traits to explain variation in male mating success suggests that other factors moderate the strength of sexual selection. Extrapair paternity is common in vertebrates and can contribute to variation in mating success and thus serves as a model for understanding the operation of sexual selection. We developed a spatially explicit, multifactor model of all possible female-male pairings to test the hypothesis that ecological (food availability) and social (breeding density, breeding distance, and the social mate's nest stage) factors influence an individual's opportunity for extrapair paternity in a socially monogamous bird, the black-throated blue warbler, Setophaga caerulescens. A male's probability of siring extrapair young decreased with increasing distance to females, breeding density, and food availability. Males on food-poor territories were more likely to sire extrapair young, and these offspring were produced farther from the male's territory relative to males on food-abundant territories. Moreover, males sired extrapair young mostly during their social mates' incubation stage, especially males on food-abundant territories. This study demonstrates how ecological and social conditions constrain the spatial and temporal opportunities for extrapair paternity that affect variation in mating success and the strength of sexual selection in socially monogamous species.

An experimental test of the effect of brood size on glucocorticoid responses, parental investment, and offspring phenotype.

Because elevated glucocorticoid levels can impair reproduction, populations or species that engage in particularly valuable reproductive attempts may down-regulate the glucocorticoid stress response during reproduction (the brood value hypothesis). It is not clear, however, whether individuals rapidly modulate glucocorticoid responses based on shifting cues about the likelihood of reproductive success. By manipulating brood size to create broods that differed in potential value, we tested whether female barn swallows (Hirundo rustica) rapidly modulated the glucocorticoid stress response to promote investment in high-value broods, and whether nestling phenotype was influenced by treatment. Within-individual changes in female corticosterone, body mass, and measures of oxidative stress were unrelated to brood size treatment. Standard offspring provisioning rate did not differ across treatments; however, in the presence of a model predator, females raising enlarged broods maintained higher offspring feeding rates relative to control broods. Brood size did influence nestling phenotype. Nestlings from enlarged broods had lower body mass and higher baseline corticosterone than those from reduced broods. Finally, in adult females both baseline and stress-induced corticosterone were individually repeatable. Thus, while under moderately challenging environmental conditions brood size manipulations had context-dependent effects on parental investment, and influenced nestling phenotype, maternal glucocorticoid levels were not modulated based on brood value but were individually consistent features of phenotype during breeding.

A comparative assessment of SNP and microsatellite markers for assigning parentage in a socially monogamous bird.

Single-nucleotide polymorphisms (SNPs) are preferred over microsatellite markers in many evolutionary studies, but have only recently been applied to studies of parentage. Evaluations of SNPs and microsatellites for assigning parentage have mostly focused on special cases that require a relatively large number of heterozygous loci, such as species with low genetic diversity or with complex social structures. We developed 120 SNP markers from a transcriptome assembled using RNA-sequencing of a songbird with the most common avian mating system-social monogamy. We compared the effectiveness of 97 novel SNPs and six previously described microsatellites for assigning paternity in the black-throated blue warbler, Setophaga caerulescens. We show that the full panel of 97 SNPs (mean Ho  = 0.19) was as powerful for assigning paternity as the panel of multiallelic microsatellites (mean Ho  = 0.86). Paternity assignments using the two marker types were in agreement for 92% of the offspring. Filtering individual samples by a 50% call rate and SNPs by a 75% call rate maximized the number of offspring assigned with 95% confidence using SNPs. We also found that the 40 most heterozygous SNPs (mean Ho  = 0.37) had similar power to assign paternity as the full panel of 97 SNPs. These findings demonstrate that a relatively small number of variable SNPs can be effective for parentage analyses in a socially monogamous species. We suggest that the development of SNP markers is advantageous for studies that require high-throughput genotyping or that plan to address a range of ecological and evolutionary questions.

Identification and characterization of microsatellite loci in two socially complex old world tropical babblers (Family Timaliidae).

BACKGROUND: Although the highest diversity of birds occurs in tropical regions, little is known about the genetic mating systems of most tropical species. We describe microsatellite markers isolated in the chestnut-crested yuhina (Staphida everetti), endemic to the island of Borneo, and the grey-throated babbler (Stachyris nigriceps), widely distributed across Southeast Asia. Both species belong to the avian family Timaliidae and are highly social, putatively cooperatively breeding birds in which helpers attend the nests of members of their social group. We obtained DNA from individuals in social groups breeding in Kinabalu Park, Malaysian Borneo. RESULTS: We used a shotgun sequencing approach and 454-technology to identify 36 microsatellite loci in the yuhina and 40 in the babbler. We tested 13 primer pairs in yuhinas and 20 in babblers and characterized eight polymorphic loci in 20 unrelated female yuhinas and 21 unrelated female babblers. Polymorphism at the yuhina loci ranged from 3 to 9 alleles, observed heterozygosities from 0.58 to 1.00, and expected heterozygosities from 0.64 to 0.81. Polymorphism at the babbler loci ranged from 3 to 12 alleles, observed heterozygosities from 0.14 to 0.90 and expected heterozygosities from 0.14 to 0.87. One locus in the yuhina deviated significantly from Hardy-Weinberg equilibrium. We detected nonrandom allele associations between two pairs of microsatellite loci in each species. CONCLUSIONS: Microsatellite markers will be used to describe the genetic mating system of these socially complex species and to measure genetic parentage and relatedness within social groups.

Experimental food supplementation reveals habitat-dependent male reproductive investment in a migratory bird.

Environmental factors can shape reproductive investment strategies and influence the variance in male mating success. Environmental effects on extrapair paternity have traditionally been ascribed to aspects of the social environment, such as breeding density and synchrony. However, social factors are often confounded with habitat quality and are challenging to disentangle. We used both natural variation in habitat quality and a food supplementation experiment to separate the effects of food availability-one key aspect of habitat quality-on extrapair paternity (EPP) and reproductive success in the black-throated blue warbler, Setophaga caerulescens. High natural food availability was associated with higher within-pair paternity (WPP) and fledging two broods late in the breeding season, but lower EPP. Food-supplemented males had higher WPP leading to higher reproductive success relative to controls, and when in low-quality habitat, food-supplemented males were more likely to fledge two broods but less likely to gain EPP. Our results demonstrate that food availability affects trade-offs in reproductive activities. When food constraints are reduced, males invest in WPP at the expense of EPP. These findings imply that environmental change could alter how individuals allocate their resources and affect the selective environment that drives variation in male mating success.

Warm springs, early lay dates, and double brooding in a North American migratory songbird, the black-throated blue warbler.

Numerous studies have correlated the advancement of lay date in birds with warming climate trends, yet the fitness effects associated with this phenological response have been examined in only a small number of species. Most of these species--primarily insectivorous cavity nesters in Europe--exhibit fitness declines associated with increasing asynchrony with prey. Here, we use 25 years of demographic data, collected from 1986 to 2010, to examine the effects of spring temperature on breeding initiation date, double brooding, and annual fecundity in a Nearctic-Neotropical migratory songbird, the black-throated blue warbler (Setophaga caerulescens). Data were collected from birds breeding at the Hubbard Brook Experimental Forest, New Hampshire, USA, where long-term trends toward warmer springs have been recorded. We found that black-throated blue warblers initiated breeding earlier in warmer springs, that early breeders were more likely to attempt a second brood than those starting later in the season, and that double brooding and lay date were linked to higher annual fecundity. Accordingly, we found selection favored earlier breeding in most years. However, in contrast to studies of several other long-distance migratory species in Europe, this selection pressure was not stronger in warmer springs, indicating that these warblers were able to adjust mean lay date appropriately to substantial inter-annual variation in spring temperature. Our results suggest that this North American migratory songbird might not experience the same fecundity declines as songbirds that are unable to adjust their timing of breeding in pace with spring temperatures.