Arrival date and territorial behavior are associated with corticosterone metabolite levels in a migratory bird

Glucocorticoids promote the mobilization of energy stores and they may facilitate the expression of energetically expensive functions. Early arrival on the breeding grounds in migratory species and territorial competition are energetically demanding activities that may be supported by elevated baseline glucocorticoid levels. Here, we evaluated the associations between the baseline levels of excreted corticosterone (CORT) metabolites of male Pied Flycatchers (Ficedula hypoleuca) just after arriving on their breeding area and timing of arrival, considering ornamental traits indicative of social status, like forehead patch size and black plumage coloration, as well as heat shock protein levels (HSP60). We observed a positive association of CORT metabolites with HSP60 levels, which are synthesized under several environmental challenges affecting cell homeostasis. Our data showed a negative association between arrival date and CORT metabolite levels, possibly as a result of the higher energetic demands imposed by the hard environmental conditions experienced at the time of an early arrival after migration. We observed a negative relationship of forehead patch dimensions and CORT metabolite levels, suggesting that dominance is associated with low baseline CORT metabolites. Also, males that expressed a higher degree of territorial behaviour when exposed to a playback song of a conspecific at their nest-box showed higher CORT metabolites upon arrival than males that expressed a lower degree of territorial behavior. This may indicate that elevated baseline CORT metabolite levels may facilitate an intense territorial competition in males. Thus, male–male competition may be a factor affecting observed baseline glucocorticoid levels in migratory birds.     

Recent northward range expansion promotes song evolution in a passerine bird,the Light‐vented Bulbul

In common with human speech, song is culturally inherited in oscine passerine birds (‘songbirds’). Intraspecific divergence in birdsong, such as development of local dialects, might be an important early step in the speciation process. It is therefore vital to understand how songs diverge, especially in founding populations. The northward expansion of the Light‐vented Bulbul Pycnonotus sinensis (J. F. Gmelin, 1789) into north China in the last 30 years provides an excellent opportunity to study birdsong evolution. We compared ~4400 songs from newly established northern populations with ~2900 songs from southern populations to evaluate song divergence after recent expansion. The total pool of syllables and especially song types was considerably smaller in the north than in the south, indicating ‘founder effects’ in the new population. The ancestral pattern of mosaic song dialects changed into a pattern of wide geographical sharing of a few song types and syllables, likely the result of fewer geographical barriers to ‘meme flow’, and the recent spread across a large area in the north. Our results suggest that song evolution and vocal trait shifts can arise rapidly after range expansion, and that in the Light‐vented Bulbul ‘founder effects’, geographical isolation, and recent rapid expansions played important roles in the evolution of song dialects.     

Variation in the hematocrit of a passerine bird across life stages is mainly of environmental origin

The heritability of the hematocrit in adult, breeding pied flycatchers Ficedula hypoleuca is examined in a southern European population across seven years to see the consistency, or lack thereof, of patterns found with the trait at fledgling age where no significant heritability could be detected. While the across-years repeatability of the trait in adult, breeding birds was low but significant, heritabilities based on adult parent-adult offspring regressions controlling for assortative mating and full-sibling comparisons did not differ significantly from zero. Neither were heritability estimates affected by selection on fledgling hematocrit, as it was unrelated to local recruitment. There was no relationship between fledgling and adult hematocrit, suggesting that both behave as phenotypically plastic, different traits. This is the first study testing for the heritability of a physiological trait in birds with data from adult, free-ranging individuals.     

Marine lifestyle is associated with higher baseline corticosterone levels in birds

Because seawater is hyperosmotic relative to body fluids of most vertebrates, marine lifestyle is expected to strongly influence the physiology of marine tetrapods. Regulating the salt content of body fluids is energetically costly; and osmoregulatory organs may not totally overcome salt load and/or water loss. As a consequence, marine lifestyle should influence physiological systems involved in the maintenance of the physiological balance (homeostasis), in the mobilisation of energetic resources (e.g., to fuel salt excretion), or in the acquisition of resources (e.g., fresh water). Corticosterone (CORT) is one such ‘generalist’ mediator that is linked with energy expenditure, physiological stress and that activates osmoregulation. As a consequence, CORT is expected to be overall higher in marine tetrapods but this hypothesis has never been tested. Using comparative analyses, we tested this hypothesis in birds, a lineage for which available data on baseline CORT allow comparing marine versus terrestrial species, and species with or without salt glands. We found that marine species (and species with salt glands) display significantly higher baseline CORT during the wintering (but not the breeding) stage. Although salt glands’ presence was tightly linked to phylogeny, our results suggest that marine lifestyle may impose a strong, but overlooked, influence on the allostasis‐related physiology of marine birds. Such habitat‐related variation in physiology is a major phenomenon to explore owing to its general implications for understanding the physiological basis of evolutionary transitions in habitat use. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 154–161.     

Hormone levels predict individual differences in reproductive success in a passerine bird

Hormones mediate major physiological and behavioural components of the reproductive phenotype of individuals. To understand basic evolutionary processes in the hormonal regulation of reproductive traits, we need to know whether, and during which reproductive phases, individual variation in hormone concentrations relates to fitness in natural populations. We related circulating concentrations of prolactin and corticosterone to parental behaviour and reproductive success during both the pre-breeding and the chick-rearing stages in both individuals of pairs of free-living house sparrows, Passer domesticus. Prolactin and baseline corticosterone concentrations in pre-breeding females, and prolactin concentrations in pre-breeding males, predicted total number of fledglings. When the strong effect of lay date on total fledgling number was corrected for, only pre-breeding baseline corticosterone, but not prolactin, was negatively correlated with the reproductive success of females. During the breeding season, nestling provisioning rates of both sexes were negatively correlated with stress-induced corticosterone levels. Lastly, individuals of both sexes with low baseline corticosterone before and high baseline corticosterone during breeding raised the most offspring, suggesting that either the plasticity of this trait contributes to reproductive success or that high parental effort leads to increased hormone concentrations. Thus hormone concentrations both before and during breeding, as well as their seasonal dynamics, predict reproductive success, suggesting that individual variation in absolute concentrations and in plasticity is functionally significant, and, if heritable, may be a target of selection.     

Nomadism and seasonal range expansion in a large frugivorous bird

Studies on the ranging behaviour of birds often suggest that ranges vary seasonally with larger ranges in the non‐breeding compared to the breeding season. However, due to limitations in tracking methods very little is known about the underlying processes driving seasonal differences in ranging behaviour, especially in fragmented, heterogeneous landscapes. Such knowledge is particularly important if movements deliver essential ecosystem functions such as seed dispersal. We contrasted the daily ranging behaviour between the breeding and non‐breeding season of a frugivorous bird and demonstrate how larger seasonal ranges in the non‐breeding season emerge through switching from a stationary home range behaviour to nomadism. We tracked movements of 29 male trumpeter hornbills Bycanistes bucinator across a fragmented landscape of eastern South Africa during different breeding and non‐breeding seasons using high temporal resolution GPS data‐loggers. Birds in the breeding seasons showed a typical, stationary home range pattern. In the non‐breeding seasons birds, rather than expanding their stationary daily ranges, switched to nomadic movements that were characterized by shifts of the general location of daily ranges to a different area every couple of days. We also found that during the breeding seasons hornbills were mostly located in large continuous forests; birds in the non‐breeding seasons frequently used forest patches within the agricultural landscape and residential areas. These seasonal differences in the movement behaviour of trumpeter hornbills may have important consequences for seed dispersal of plant species. Our findings show how seasonal range expansion of frugivorous birds may be driven by fundamental behavioural changes that have important consequences for ecosystem processes.     

Gene flow and range expansion in a mountain‐dwelling passerine with a fragmented distribution

We studied gene flow and bottleneck events in the population history of locally isolated citril finches endemic to European mountains. For the present study, we used two genetic markers with different rates of evolution: a fast evolving mitochondrial marker (ATPase6/8) and a more slowly evolving nuclear marker (02401). Populations north of the Pyrenees showed in general fewer haplotypes and a considerable lower nucleotide and gene diversity than the Iberian populations. Unexpectedly, we found very little genetic variability in the fast evolving mitochondrial marker, arguing for a strong and relatively recent bottleneck event in the species population history. This pattern potentially reflects a sudden decrease of crucial resources during Mid‐Holocene (mountain pine, Scots pine, and black pine) and a subsequent breakdown of the population. The bottleneck could also have been caused or coincide with a selective sweep in the mitochondrion. By contrast, the slowly evolving nuclear marker showed a much higher variability. This marker probably reflects major gene flow along a potential expansion pathway from the Eastern Pyrenees, northwards to the populations of Central Europe, and southwards to the more fragmented populations of central and southern Spain. The population of the Western Pyrenees (Navarra) appears to be cut‐off from this major gene flow and our data indicate a certain degree of partial isolation, probably reflecting more ancient events (e.g. the separation in distinct refuge sites during the last glacial maximum). © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 707–721.     

Functional infertility in a wild passerine bird

Information about male infertility in free‐living bird populations and its underlying causes are poorly documented in the literature. Here, we assessed sperm quality and infertility among males in a wild population of Blue Tits Cyanistes caeruleus, a socially monogamous passerine with frequent extra‐pair mating. One of 30 males (3.3%) studied across two breeding seasons had morphologically abnormal and nearly immotile spermatozoa in combination with zero annual fertilization success. Demonstration of male functional infertility suggests the possibility that socially monogamous females of the study population could obtain a direct fitness benefit by mating polyandrously to increase fertilization success, which could contribute to selection on extra‐pair mating behaviour.     

Context-dependent vocal mimicry in a passerine bird

How do birds select the sounds they mimic, and in what contexts do they use vocal mimicry? Some birds show a preference for mimicking other species' alarm notes, especially in situations when they appear to be alarmed. Yet no study has demonstrated that birds change the call types they mimic with changing contexts. We found that greater racket-tailed drongos (Dicrurus paradiseus) in the rainforest of Sri Lanka mimic the calls of predators and the alarm-associated calls of other species more often than would be expected from the frequency of these sounds in the acoustic environment. Drongos include this alarm-associated mimicry in their own alarm vocalizations, while incorporating other species' songs and contact calls in their own songs. Drongos show an additional level of context specificity by mimicking other species' ground predator-specific call types when mobbing. We suggest that drongos learn other species' calls and their contexts while interacting with these species in mixed flocks. The drongos' behaviour demonstrates that alarm-associated calls can have learned components, and that birds can learn the appropriate usage of calls that encode different types of information.     

Rapid changes in phenotype distribution during range expansion in a migratory bird

The capacity of species to track changing environmental conditions is a key component of population and range changes in response to environmental change. High levels of local adaptation may constrain expansion into new locations, while the relative fitness of dispersing individuals will influence subsequent population growth. However, opportunities to explore such processes are rare, particularly at scales relevant to species-based conservation strategies. Icelandic black-tailed godwits, Limosa limosa islandica, have expanded their range throughout Iceland over the last century. We show that current male morphology varies strongly in relation to the timing of colonization across Iceland, with small males being absent from recently occupied areas. Smaller males are also proportionately more abundant on habitats and sites with higher breeding success and relative abundance of females. This population-wide spatial structuring of male morphology is most likely to result from female preferences for small males and better-quality habitats increasing both small-male fitness and the dispersal probability of larger males into poorer-quality habitats. Such eco-evolutionary feedbacks may be a key driver of rates of population growth and range expansion and contraction.     

Variation of basal EROD activities in ten passerine bird species--relationships with diet and migration status

Inter-specific differences in animal defence mechanisms against toxic substances are currently poorly understood. The ethoxyresorufin-O-deethylase (EROD) enzyme plays an important role in defence against toxic chemicals in a wide variety of animals, and it is an important biomarker for environmental contamination. We compared basal hepatic EROD activity levels among ten passerine species to see if there is inter-specific variation in enzyme activity, especially in relation to their diet and migration status. Migratory insectivores showed higher EROD activity compared to granivores. We hypothesize that the variable invertebrate diet of migratory insectivores contains a wider range of natural toxins than the narrower diet of granivores. This may have affected the evolution of mixed function oxidases (MFO) system and enzyme activities. We further tested whether metabolic rates or relative liver size were associated with the variation in detoxification capacity. We found no association between EROD activity and relative (per mass unit) basal metabolic rate (BMR). Instead, EROD activity and relative liver mass (% of body mass) correlated positively, suggesting that a proportionally large liver also functions efficiently. Our results suggest that granivores and non-migratory birds may be more vulnerable to environmental contaminants than insectivores and migratory birds. The diet and migration status, however, are phylogenetically strongly connected to each other, and their roles cannot be fully separated in our analysis with only ten passerine species.     

Niche expansion leads to small-scale adaptive divergence along an elevation gradient in a medium-sized passerine bird

Niche expansion can lead to adaptive differentiation and speciation, but there are few examples from contemporary niche expansions about how this process is initiated. We assess the consequences of a niche expansion by Mexican jays (Aphelocoma ultramarina) along an elevation gradient. We predicted that jays at high elevation would have straighter bills adapted to feeding on pine cones, whereas jays at low elevation would have hooked bills adapted to feeding on acorns. We measured morphological and genetic variation of 95 adult jays and found significant differences in hook length between elevations in accordance with predictions, a pattern corroborated by analysis at the regional scale. Genetic results from microsatellite and mtDNA variation support phenotypic differentiation in the presence of gene flow coupled with weak, but detectable genetic differentiation between high- and low-elevation populations. These results demonstrate that niche expansion can lead to adaptive divergence despite gene flow between parapatric populations along an elevation gradient, providing information on a key precursor to ecological speciation.     

Novel variation associated with species range expansion

When species shift their ranges to track climate change, they are almost certain to experience novel environments to which they are poorly adapted. Otaki and co-workers document an explosion of wing pattern variation accompanying range expansion in the pale grass blue butterfly. This pattern can be replicated in the laboratory using artificial selection on cold shocked pupae, at temperature extremes typical of recently colonized environments. We discuss how this phenotypic plasticity may be associated with successful colonization and how significant local adaptation is likely to re-establish developmental control. Integrating knowledge of trait plasticity into current genetic models of adaptation is central to our understanding of when and where a colonising population will be able to persist and adapt in novel surroundings.     

Footedness predicts escape performance in a passerine bird

Behavioral lateralization, which is associated with the functional lateralization of the two brain hemispheres, commonly exists in animals and can provide an individual with benefits such as enhanced cognition and dual tasking. Lateral bias in limb use, as a type of behavioral lateralization, occur in many species, but the reasons for the coexistence of left‐ and right‐biased individuals in a population remain poorly understood. We examined the footedness of male yellow‐bellied tits (Pardaliparus venustulus) when they used feet to clamp mealworms against a perch, and tested its association with other fitness‐related behavioral traits (i.e., feeding efficiency, exploration tendency, and escape performance). We expected differently footed individuals to have respective advantages in these behaviors and thereby coexist (“respective advantage” hypothesis). We found their footedness repeatable, and there was no population‐level bias. While no associations of feeding efficiency and exploration tendency with footedness were detected, the right‐footed individuals were found to be harder to catch than the other individuals. Future studies need to investigate the reasons for the right‐footed individuals' superior escape performance. Moreover, the escape advantage for being right‐footed and the lack of population‐level bias in footedness in male yellow‐bellied tits suggest that the benefits related to left footedness also remain to be explored.     

Heritability of parental effort in a passerine bird

Abstract The study of the evolution of parental care is central to our understanding of social systems, sexual selection, and interindividual conflict, yet we know virtually nothing about the genetic architecture of parental care traits in natural populations. In this paper, we use data from a long term field study of a passerine bird, the long-tailed tit ( Aegithalos caudatus ), to examine the heritability of the rate at which parents feed offspring. This measure of effort is positively related to offspring survival, is repeatable within individuals, and does not appear to be confounded by environmental effects. Using both parent-offspring regression, and an animal model approach, with a pedigree derived from ringing data, we show that our measure of effort has a significant heritable component.     

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

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.

     

Postglacial colonisation patterns and the role of isolation and expansion in driving diversification in a passerine bird

Pleistocene glacial cycles play a major role in diversification and speciation, although the relative importance of isolation and expansion in driving diversification remains debated. We analysed mitochondrial DNA sequence data from 15 great reed warbler (Acrocephalus arundinaceus) populations distributed over the vast Eurasian breeding range of the species, and revealed unexpected postglacial expansion patterns from two glacial refugia. There were 58 different haplotypes forming two major clades, A and B. Clade A dominated in Western Europe with declining frequencies towards Eastern Europe and the Middle East, but showed a surprising increase in frequency in Western and Central Asia. Clade B dominated in the Middle East, with declining frequencies towards north in Central and Eastern Europe and was absent from Western Europe and Central Asia. A parsimonious explanation for these patterns is independent postglacial expansions from two isolated refugia, and mismatch distribution analyses confirmed this suggestion. Gene flow analyses showed that clade A colonised both Europe and Asia from a refugium in Europe, and that clade B expanded much later and colonised parts of Europe from a refugium in the Middle East. Great reed warblers in the eastern parts of the range have slightly paler plumage than western birds (sometimes treated as separate subspecies; A. a. zarudnyi and A. a. arundinaceus, respectively) and our results suggest that the plumage diversification took place during the easterly expansion of clade A. This supports the postglacial expansion hypothesis proposing that postglacial expansions drive diversification in comparatively short time periods. However, there is no indication of any (strong) reproductive isolation between clades and our data show that the refugia populations became separated during the last glaciation. This is in line with the Pleistocene speciation hypothesis invoking that much longer periods of time in isolation are needed for speciation to occur.     

Storms drive altitudinal migration in a tropical bird

Although migration is a widespread and taxonomically diverse behaviour, the ecological factors shaping migratory behaviour are poorly understood. Like other montane taxa, many birds migrate along elevational gradients in the tropics. Forty years ago, Alexander Skutch postulated that severe storms could drive birds to migrate downhill. Here, we articulate a novel mechanism that could link storms to mortality risks via reductions in foraging time and provide, to our knowledge, the first tests of this hypothesis in the White-ruffed Manakin (Corapipo altera), a small partially migratory frugivore breeding on the Atlantic slope of Costa Rica. As predicted, variation in rainfall was associated with plasma corticosterone levels, fat stores, plasma metabolites and haematocrit. By collecting data at high and low elevation sites simultaneously, we also found that high-elevation residents were more adversely affected by storms than low elevation migrants. These results, together with striking temporal capture patterns of altitudinal migrants relative to storms, provide, to our knowledge, the first evidence that weather-related risks incurred by species requiring high food intake rates can explain altitudinal migrations of tropical animals. These findings resolve conflicting evidence for and against food limitation being important in the evolution of this behaviour, and highlight how endogenous and exogenous processes influence life-history trade-offs made by individuals in the wild. Because seasonal storms are a defining characteristic of most tropical ecosystems and rainfall patterns will probably change in ensuing decades, these results have important implications for understanding the ecology, evolution and conservation of tropical animals.