Increased extra‐pair paternity in broods of aging males and enhanced recruitment of extra‐pair young in a migratory bird

Despite keen interest in extra‐pair mating in birds, its adaptive significance remains unresolved. Here, we use a multi‐year dataset to test whether traits of a female's social mate influence her propensity to produce extra‐pair offspring in a population of house wrens, and whether producing extra‐pair young has consequences for a female's fitness through effects on offspring survival. Females were most likely to produce extra‐pair offspring when paired with old males and when paired with males on poor‐quality territories, although this latter effect was marginally nonsignificant. Among offspring, the cutaneous immunity of within‐pair young decreased as the age of their sires increased, but cutaneous immunity of extra‐pair young was not affected by the age of their extra‐pair sires or by the age of the males rearing them. Extra‐pair offspring were more likely than within‐pair offspring to return as breeding adults to the local population, with extra‐pair sons being more likely to return as a breeder for multiple years. Our findings support the hypothesis that females produce extra‐pair offspring to enhance their inclusive fitness beyond what they are capable of given the male with which they are socially paired.     

Spatial and temporal variation in population trends in a long‐distance migratory bird

Aim Over the past three decades, evidence has been growing that many Afro‐Palaearctic migratory bird populations have suffered sustained and severe declines. As causes of these declines exist across both the breeding and non‐breeding season, identifying potential drivers of population change is complex. In order to explore the roles of changes in regional and local environmental conditions on population change, we examine spatial and temporal variation in population trajectories of one of Europe’s most abundant Afro‐Palaearctic summer migrants, the willow warbler, Phylloscopus trochilus. Location Britain and Ireland. Methods We use national survey data from Britain and Ireland (BBS: BTO/RSPB/JNCC Breeding Bird Survey and CBS: BWI/NPWS/Heritage Council Countryside Breeding Survey) from 1994 to 2006 to model the spatial and temporal variation in willow warbler population trends. Results Across Britain and Ireland, population trends follow a gradient from sharp declines in the south and east of England to shallow declines and/or slight increases in parts of north and west England, across Scotland and Ireland. Decreasing the spatial scale of analysis reveals variation in both the rate and spatial extent of population change within central England and the majority of Scotland. The rates of population change also vary temporally; declines in the south of England are shallower now than at the start of the time series, whereas populations further north in Britain have undergone periods of increase and decline. Main conclusion These patterns suggest that regional‐scale drivers, such as changing climatic conditions, and local‐scale processes, such as habitat change, are interacting to produce spatially variable population trends. We discuss the potential mechanisms underlying these interactions and the challenges in addressing such changes at scales relevant to migratory species.     

Large‐scale geographic variation in iridescent structural ornaments of a long‐distance migratory bird

Iridescent colours produced during moult likely play an important role in pair formation in birds. We sought to quantify geographic variation in such colouration in a duck species, Eurasian teal Anas crecca, in winter (when mating occurs) to evaluate whether this variation reflects birds’ breeding origins or differential individual migration strategies in both males and females. We combined information on feather production region and individual attributes (body size, sex and age) of Eurasian teal from 82 wintering sites in France. Feather production region (moult site or natal origin) was inferred using feather deuterium values (δD_f). We performed spectral measurements to evaluate speculum colour and brightness contrasts for 1052 teal collected over four years. Colouration differed strongly among wintering regions, with birds wintering in eastern France exhibiting higher colour contrast than those wintering in the west. Body size and colouration were positively related. There were no differences in cohort‐specific δD_f values between separate wintering regions in France, indicating that within a winter quarter teal originated from areas across the entire breeding range. Overall, patterns of spatial variation in feather colouration were related most closely to body size which was consistent with predictions of a differential migration hypothesis, with larger and more colour‐contrasting birds wintering closer to their breeding grounds. Because moult speed is also known to affect colour production, early breeders or individuals that skipped reproduction may have invested more or earlier in their feather quality to gain potential advantages in monopolizing future mates.     

Large brain size is associated with low extra‐pair paternity across bird species

BackgroundGaining extrapair copulations (EPCs) is a complicated behavior process. The interaction between males and females to procure EPCs may be involved in brain function evolution and lead to a larger brain. Thus, we hypothesized that extrapair paternity (EPP) rate can be predicted by relative brain size in birds. Past work has implied that the EPP rate is associated with brain size, but empirical evidence is rare.MethodsWe collated data from published references on EPP levels and brain size of 215 bird species to examine whether the evolution of EPP rate can be predicted by brain size using phylogenetically generalized least square (PGLS) models and phylogenetic path analyses.ResultsWe found that EPP rates (both the percentage EP offspring and percentage of broods with EP offspring) are negatively associated with relative brain size. We applied phylogenetic path analysis to test the causal relationship between relative brain size and EPP rate. Best‐supported models (ΔCICc < 2) suggested that large brain lead to reduced EPP rate, which failed to support the hypothesis that high rates of EPP cause the evolution of larger brains.ConclusionThis study indicates that pursuing EPCs may be a natural instinct in birds and the interaction between males and females for EPCs may lead to large brains, which in turn may restrict their EPC level for both sexes across bird species.     

Increase in protandry over time in a long‐distance migratory bird

Protandry is a widespread life‐history phenomenon describing how males precede females at the site or state of reproduction. In migratory birds, protandry has an important influence on individual fitness, the migratory syndrome, and phenological response to climate change. Despite its significance, accurate analyses on the dynamics of protandry using data sets collected at the breeding site, are lacking. Basing our study on records collected during two time periods, 1979 to 1988 and 2006 to 2016, we aim to investigate protandry dynamics over 38 years in a breeding population of willow warblers (Phylloscopus trochilus). Change in the timing of arrival was analyzed in males and females, and protandry (number of days between male and female arrival) was investigated both at population level and within breeding pairs. Our results show advancement in the arrival time at the breeding site in both sexes, but male arrival has advanced to a greater extent, leading to an increase in protandry both at the population level and within breeding pairs. We did not observe any change in sex ratio that could explain the protandry increase, but pronounced temperature change has occurred and been reported in the breeding area and along the migratory route. Typically, natural selection opposes too early arrival in males, but given warmer springs, this counteracting force may be relaxing, enabling an increase in protandry. We discuss whether our results suggest that climate change has induced sex‐specific effects, if these could be evolutionary and whether the timing of important life‐history stages such as arrival at the breeding site may change at different rates in males and females following environmental shifts.     

Form,function and consequences of density dependence in a long‐distance migratory bird

The density dependence of demographic parameters and its implications for population regulation have long been recognized. Recent work has revealed potential effects of density on mating systems and sexual selection, but few studies concurrently assess the consequences of density on both demography and sexual selection. Such an approach is important because population processes and individual behaviors can interact to influence population growth and evolutionary trajectories. In this study, we tested the density dependence of breeding success, extra‐pair paternity, and the opportunity for sexual selection in a population of American redstarts Setophaga ruticilla using two different measures of density. To evaluate temporal patterns, we analyzed annual territory density, based on the total number of territories at our study site each year. To evaluate spatial patterns, we analyzed local territory density within years, based on the number of territories surrounding a focal territory. Greater annual density was associated with fewer offspring fledged per female, a reduced mean population rate of fledging success, and a lower relative contribution of extra‐pair paternity to male fitness. Greater local density was associated with fewer offspring fledged, reduced fledgling success, higher rates of nest loss, and higher rates of paternity loss on focal territories. Interestingly, greater local density was also associated with greater nestling mass on focal territories, which could imply that more densely‐packed territories contain superior resources. Overall, our results suggest that the effects of crowding via greater territory density reduce fecundity through increased nest predation, rather than reduced food availability, and increase rates of extra‐pair paternity. Thus, the selective pressures faced by individuals and their reproductive behaviors are likely to differ based on the annual and local density they experience, which may then feed back into population demography.     

Longitudinal data reveal ontogenetic changes in the wing morphology of a long‐distance migratory bird

In migratory bird species, juveniles normally have shorter and more rounded wings than adults. The causes of this age‐specific difference in wing morphology, however, are largely unknown. Here, we used longitudinal data collected over 3 years from a Pied Flycatcher Ficedula hypoleuca population to assess whether age‐related differences in wing morphology are a consequence of ontogenetic changes or of selection favouring birds with longer and more pointed wings. Our study provides evidence of ontogenetic changes in wing length and shape, whereby birds grow longer and more pointed wings as they grow older. Age‐dependent variation is likely to be adaptive and may partly explain age differences in spring migration phenology and breeding success.     

Ecological mismatches are moderated by local conditions for two populations of a long‐distance migratory bird

Ecological mismatches between reproductive events and seasonal resource peaks are frequently proposed to be a key driver of population dynamics resulting from global climate change. Many local populations are experiencing reduced reproductive success as a consequence of mismatches, but few mismatches have led to species‐level population declines. To better understand this apparent paradox, we investigated the breeding phenology and chick survival of two disjunct populations of Hudsonian godwits Limosa haemastica breeding at Churchill, Manitoba and Beluga River, Alaska. Only one population experienced a mismatch: godwits bred nearly one week after the onset of the invertebrate peak at Churchill because of asynchronous climatic change occurring throughout their annual cycle. However, chicks were not uniformly affected by the mismatch — growth rates and survival of young chicks were not correlated with invertebrate abundance, but older chicks tended to suffer lower survival rates on days of low invertebrate abundance. Ecological mismatches thus resulted in a complex array of consequences, but nonetheless contributed to reductions in chick survival. In contrast, godwits at Beluga River hatched their chicks just before the invertebrate peak, such that the period of highest energetic need coincided with the period of highest invertebrate abundance. As a result, growth rates and survival of godwit chicks were unaffected by invertebrate abundance. Godwits at Beluga River were able to properly time their reproduction because of predictable rates of climatic change and strong selection imposed by high predation on late‐hatched chicks. Taken together, our results suggest that population‐specific, local‐scale selection pressures play a critical role in determining the degree and severity of ecological mismatches. The potential for global climate change to induce species‐level population declines may therefore be mediated by the spatial variation in the selection pressures acting across a species’ range.     

Migration phenology and winter habitat quality are related to circulating androgen in a long‐distance migratory bird

In migratory birds, the timing of departure from wintering grounds is often dependant on the quality of habitat on an individual's territory and may influence individual fitness, resulting in an interaction of life history stages across large geographical distances. American redstart Setophaga ruticilla males who overwinter in high quality habitats arrive early to breed and subsequently produce more offspring than late arrivers. Since many migratory species overlap vernal migration with the physiological transition to breeding, we examined if breeding preparation plays a role in this seasonal interaction. We tested the hypothesis that early arriving male redstarts from high quality winter habitats are in superior breeding condition by simultaneously measuring winter habitat quality (stable‐carbon isotopes) and breeding preparation (circulating androgen, cloacal protuberance (CP) diameter) upon arrival at breeding grounds. Compared with late arrivers, early arriving males were from higher quality winter habitats and had higher androgen, but smaller CPs. Males arriving with higher androgen were in more advanced physiological migratory condition, as measured by haematocrit. Early arrivers were more likely to successfully breed, but there was no significant relationship between androgen upon arrival and breeding success. One possible explanation for these relationships is that androgen measured during arrival is most relevant in a migratory context, such that birds with high androgen may benefit from effects on migratory condition, positively influencing fitness through earlier arrival.     

Annual variation in long‐distance dispersal driven by breeding and non‐breeding season climatic conditions in a migratory bird

Long‐distance dispersal is a fundamental process in ecology and evolution but the factors that influence these movements remain poorly understood in most species. We used stable hydrogen isotopes to quantify the rate and direction of long‐distance immigration in a breeding population of American redstarts and to test whether the settlement decisions that result in long‐distance dispersal are driven by habitat saturation or by the phenology of breeding‐season resources. Our results provide evidence that both natal dispersal and breeding dispersal were influenced by the timing of breeding‐season phenology, with both age classes more likely to disperse north in years when the onset of breeding‐season phenology occurs earlier than normal. Yearlings were also more likely to disperse north following winters with poor habitat quality on their non‐breeding grounds, demonstrating that carry‐over effects from the non‐breeding season influence natal dispersal in this species. Collectively, these results are consistent with the hypothesis that American redstarts use the phenology of breeding season resources as a cue to select breeding sites. Our results suggest that long‐distance dispersal may allow individuals to rapidly respond to advancing phenology caused by global climate change, though their ability to do so may be constrained by long‐term decline in habitat quality predicted for their tropical non‐breeding grounds.     

Heritability of arrival date in a migratory bird

The behaviour of long-distance migratory birds is assumed to partly be under the influence of genes, as demonstrated by selection experiments. Furthermore, competition for early arrival among males may lead to condition-dependent migration associated with fitness benefits of early arrival achieved by individuals in prime condition. Here I present field data on the repeatability and the heritability of arrival date in a trans-equatorial migratory bird, the barn swallow Hirundo rustica, and I test for a genetic correlation between arrival date and the expression of a condition-dependent secondary sexual character. The repeatability was statistically significant and the heritability of arrival date was estimated to be 0.54 (s.e. = 0.15). There was no significant evidence of this estimate being inflated by environmental or maternal condition during rearing. Arrival date and migration are condition dependent in the barn swallow, with males with the most exaggerated secondary sexual characters also arriving the earliest. There was a significant genetic correlation between arrival date and tail length in male barn swallows, providing indirect evidence for a genetic basis of this condition dependence. Given the high level of heritability, arrival date could readily respond to selection caused by environmental change.     

“Closer‐to‐home” strategy benefits juvenile survival in a long‐distance migratory bird

Human‐induced changes in the climate and environment that occur at an unprecedented speed are challenging the existence of migratory species. Faced with these new challenges, species with diverse and flexible migratory behaviors may suffer less from population decline, as they may be better at responding to these changes by altering their migratory behavior. At the individual level, variations in migratory behavior may lead to differences in fitness and subsequently influence the population's demographic dynamics. Using lifetime GPS bio‐logging data from 169 white storks (Ciconia ciconia), we explore whether the recently shortened migration distance of storks affects their survival during different stages of their juvenile life. We also explore how other variations in migratory decisions (i.e., time, destination), movement activity (measured using overall body dynamic acceleration), and early life conditions influence juvenile survival. We observed that their first autumn migration was the riskiest period for juvenile white storks. Individuals that migrated shorter distances and fledged earlier experienced lower mortality risks. In addition, higher movement activity and overwintering “closer‐to‐home” (with 84.21% of the tracked individuals stayed Europe or North Africa) were associated with higher survival. Our study shows how avian migrants can change life history decisions over only a few decades, and thus it helps us to understand and predict how migrants respond to the rapidly changing world.     

Female extra‐pair behavior is not associated with reduced paternal care in Thorn‐tailed Rayadito

Extra‐pair behavior is present in 76% of socially monogamous bird species with biparental care. This behavior may produce costs to females related to a reduction in paternal care. We estimated the percentage of extra‐pair offspring and quantified paternal care in 44 nests of Thorn‐tailed Rayadito (Aphrastura spinicauda) to assess whether males reduce their parental care when females obtain extra‐pair fertilizations. We used data from a sub‐Antarctic population of Rayadito located on Navarino Island (55°4′S, 67°40′W), southern Chile. We found no statistical support for a relationship between variation in paternal care and the percentage of extra‐pair offspring. We discuss how the inability of breeding males to assess their genetic paternity and potential restrictions on behavioral flexibility may explain this result. Additionally, if paternal care is subjected to sexual selection, this could limit a facultative response to female extra‐pair behavior by males. Finally, it is possible that a reduction in paternal care might not have evolved in this particular locality given the low frequency of extra‐pair paternity in our study population.     

MHC‐dependent survival in a wild population: evidence for hidden genetic benefits gained through extra‐pair fertilizations

Females should prefer to be fertilized by males that increase the genetic quality of their offspring. In vertebrates, genes of the major histocompatibility complex (MHC) play a key role in the acquired immune response and have been shown to affect mating preferences. They are therefore important candidates for the link between mate choice and indirect genetic benefits. Higher MHC diversity may be advantageous because this allows a wider range of pathogens to be detected and combated. Furthermore, individuals harbouring rare MHC alleles might better resist pathogen variants that have evolved to evade common MHC alleles. In the Seychelles warbler, females paired with low MHC‐diversity males elevate the MHC diversity of their offspring to levels comparable to the population mean by gaining extra‐pair fertilizations. Here, we investigate whether increased MHC diversity results in higher life expectancy and whether there are any additional benefits of extra‐pair fertilizations. Our 10‐year study found a positive association between MHC diversity and juvenile survival, but no additional survival advantage of extra‐pair fertilizations. In addition, offspring with a specific allele (Ase‐ua4) had a fivefold longer life expectancy than offspring without this allele. Consequently, the interacting effects of sexual selection and pathogen‐mediated viability selection appear to be important for maintaining MHC variation in the Seychelles warbler. Our study supports the prediction that MHC‐dependent extra‐pair fertilizations result in genetic benefits for offspring in natural populations. However, such genetic benefits might be hidden and not necessarily apparent in the widely used fitness comparison of extra‐ and within‐pair offspring.     

The large‐scale drivers of population declines in a long‐distance migratory shorebird

Migratory species can travel tens of thousands of kilometers each year, spending different parts of their annual cycle in geographically distinct locations. Understanding the drivers of population change is vital for conserving migratory species, yet the challenge of collecting data over entire geographic ranges has hindered attempts to identify the processes leading to observed population changes. Here, we use remotely sensed environmental data and bird count data to investigate the factors driving variability in abundance in two subspecies of a long‐distance migratory shorebird, the bar‐tailed godwit Limosa lapponica. We compiled a spatially and temporally explicit dataset of three environmental variables to identify the conditions experienced by each subspecies in each stage of their annual cycle (breeding, non‐breeding and staging). We used a Bayesian N‐mixture model to analyze 18 years of monthly count data from 21 sites across Australia and New Zealand in relation to the remote sensing data. We found that the abundance of one subspecies L. l. menzbieri in their non‐breeding range was related to climate conditions in breeding grounds, and detected sustained population declines between 1995 and 2012 in both subspecies (L. l. menzbieri, –6.7% and L. l. baueri, –2.1% year^–1). To investigate the possible causes of the declines, we quantified changes in habitat extent at 22 migratory staging sites in the Yellow Sea, East Asia, over a 25‐year period and found –1.7% and –1.2% year^–1 loss of habitat at staging sites used by L. l. menzbieri and L. l baueri, respectively. Our results highlight the need to identify environmental and anthropogenic drivers of population change across all stages of migration to allow the formulation of effective conservation strategies across entire migratory ranges.     

Multiple hypotheses explain variation in extra‐pair paternity at different levels in a single bird family

Extra‐pair paternity (EPP), where offspring are sired by a male other than the social male, varies enormously both within and among species. Trying to explain this variation has proved difficult because the majority of the interspecific variation is phylogenetically based. Ideally, variation in EPP should be investigated in closely related species, but clades with sufficient variation are rare. We present a comprehensive multifactorial test to explain variation in EPP among individuals in 20 populations of nine species over 89 years from a single bird family (Maluridae). Females had higher EPP in the presence of more helpers, more neighbours or if paired incestuously. Furthermore, higher EPP occurred in years with many incestuous pairs, populations with many helpers and species with high male density or in which males provide less care. Altogether, these variables accounted for 48% of the total and 89% of the interspecific and interpopulation variation in EPP. These findings indicate why consistent patterns in EPP have been so challenging to detect and suggest that a single predictor is unlikely to account for the enormous variation in EPP across levels of analysis. Nevertheless, it also shows that existing hypotheses can explain the variation in EPP well and that the density of males in particular is a good predictor to explain variation in EPP among species when a large part of the confounding effect of phylogeny is excluded.     

Differences in perceived predation risk associated with variation in relative size of extra‐pair and within‐pair offspring

Extra‐pair paternity (EPP) is a widespread phenomenon in birds. Researchers have long hypothesized that EPP must confer a fitness advantage to extra‐pair offspring (EPO), but empirical support for this hypothesis is definitively mixed. This could be because genetic benefits of EPP only exist in a subset of environmental contexts to which a population is exposed. From 2013 to 2015, we manipulated perceived predator density in a population of tree swallows (Tachycineta bicolor) breeding in New York to see whether fitness outcomes of extra‐pair and within‐pair offspring (WPO) varied with predation risk. In nests that had been exposed to predators, EPO were larger, longer‐winged and heavier than WPO. In nonpredator nests, WPO tended to be larger, longer‐winged and heavier than EPO, though the effect was nonsignificant. We found no differences in age, morphology or stress physiology between extra‐pair and within‐pair sires from the same nest, suggesting that additive genetic benefits cannot fully explain the differences in nestling size that we observed. The lack of an effect of predator exposure on survival or glucocorticoid stress physiology of EPO and WPO further suggests that observed size differences do not reflect more general variation in intrinsic genetic quality. Instead, we suggest that size differences may have arisen through differential investment into EPO and WPO by females, perhaps because EPO and WPO represent different reproductive strategies, with each type of nestling conferring a fitness advantage in specific ecological contexts.     

Long‐term continental changes in wing length,but not bill length,of a long‐distance migratory shorebird

We compiled a >50‐year record of morphometrics for semipalmated sandpipers (Calidris pusilla), a shorebird species with a Nearctic breeding distribution and intercontinental migration to South America. Our data included >57,000 individuals captured 1972–2015 at five breeding locations and three major stopover sites, plus 139 museum specimens collected in earlier decades. Wing length increased by ca. 1.5 mm (>1%) prior to 1980, followed by a decrease of 3.85 mm (nearly 4%) over the subsequent 35 years. This can account for previously reported changes in metrics at a migratory stopover site from 1985 to 2006. Wing length decreased at a rate of 1,098 darwins, or 0.176 haldanes, within the ranges of other field studies of phenotypic change. Bill length, in contrast, showed no consistent change over the full period of our study. Decreased body size as a universal response of animal populations to climate warming, and several other potential mechanisms, are unable to account for the increasing and decreasing wing length pattern observed. We propose that the post‐WWII near‐extirpation of falcon populations and their post‐1973 recovery driven by the widespread use and subsequent limitation on DDT in North America selected initially for greater flight efficiency and latterly for greater agility. This predation danger hypothesis accounts for many features of the morphometric data and deserves further investigation in this and other species.