The effect of environmental variation on the relationship between survival and risk-taking behaviour in a migratory songbird.

Temporal changes in environmental conditions may play a major role in the year-to-year variation in fitness consequences of behaviours. Identifying environmental drivers of such variation is crucial to understand the evolutionary trajectories of behaviours in natural contexts. However, our understanding of how environmental variation influences behaviours in the wild remains limited. Using data collected over 14 breeding seasons from a collared flycatcher (Ficedula albicollis) population, we examined the effect of environmental variation on the relationship between survival and risk-taking behaviour, a highly variable behavioural trait with great evolutionary and ecological significance. Specifically, using annual recapture probability as a proxy of survival, we evaluated the specific effect of predation pressure, food availability and mean temperature on the relationship between annual recapture probability and risk-taking behaviour (measured as flight initiation distance, FID). We found a negative trend, as the relationship between annual recapture probability and FID decreased over the study years, and changed from positive to negative. Specifically, in the early years of the study, risk-avoiding individuals exhibited a higher annual recapture probability, whereas in the later years, risk-avoiders had a lower annual recapture probability. However, we did not find evidence that any of the considered environmental factors mediated the variation in the relationship between survival and risk-taking behaviour.

High diversity, novel genotypes, and vertical transmission of hemotropic Mycoplasma in micromammals.

Hemotropic mycoplasmas (hemoplasmas) are emerging zoonotic pathogens. Micromammals have received little attention as hosts for hemoplasmas despite their ubiquitous presence, high population abundances, and close association with humans. A PCR protocol targeting a fragment of the 16 S rRNA gene and direct sequencing in blood samples of 189 adult specimens and 35 fetuses belonging to three species of Eulipotyphla (shrews) and seven species of Rodentia, captured in three ecologically diverse habitats in North-Eastern Spain (Steppe, High Mountain, Mediterranean) yielded and occurrence of 26%, including 36% of 39 shrews and 23% of 150 rodents. Sequencing revealed the presence of 14 nucleotide sequence types (ntST) among the 56 readable sequences. In general, each ntST was associated with a given host species, although in some cases, the same ntST was sequenced in different species (chiefly rodents). Most ntST were closely related to rodent and/or bat hemoplasmas, but one was identical with Mycoplasma haemocanis/haemofelis, and others can be considered novel genotypes. High sequence diversity was detected in rodents, whereas in the white-toothed shrew (Crocidura russula), 9/11 sequences from two distant areas were identical. Phylogenetic and network analyses classified our sequences in different clades including hemoplasmas of rodents, carnivores, bats, and humans. Twelve of the fetuses (34.2%) of 9/12 litters (75.0%) of shrews and rodents were hemoplasma-positive, indicating frequent vertical transmission. Our study contributes to expanding our knowledge about the distribution, diversity, and transmission of hemoplasmas.

Genetic footprints of a rapid and large-scale range expansion: the case of cyclic common vole in Spain.

In the Anthropocene, many species are rapidly shifting their ranges in response to human-driven habitat modifications. Studying patterns and genetic signatures of range shifts helps to understand how species cope with environmental disturbances and predict future shifts in the face of global environmental change. We investigated the genetic signature of a contemporary wide-range expansion observed in the Iberian common vole Microtus arvalis asturianus shortly after a colonization event. We used mtDNA and microsatellite data to investigate patterns of genetic diversity, structure, demography, and gene flow across 57 localities covering the historical range of the species and the newly colonized area. The results showed a genetic footprint more compatible with a true range expansion (i.e. the colonization of previously unoccupied areas), than with a model of "colonization from within" (i.e. local expansions from small, unnoticed populations). Genetic diversity measures indicated that the source population was likely located at the NE of the historical range, with a declining gradient of genetic diversity towards the more recently invaded areas. At the expansion front, we observed the greatest gene flow and smallest pairwise differences between nearby localities. Both natural landscape features (rivers) and recent anthropogenic barriers (roads, railways) explained a large proportion of genetic variance among populations and had a significant impact on the colonization pathways used by voles.

Temperature synchronizes temporal variation in laying dates across European hole-nesting passerines.

Identifying the environmental drivers of variation in fitness-related traits is a central objective in ecology and evolutionary biology. Temporal fluctuations of these environmental drivers are often synchronized at large spatial scales. Yet, whether synchronous environmental conditions can generate spatial synchrony in fitness-related trait values (i.e., correlated temporal trait fluctuations across populations) is poorly understood. Using data from long-term monitored populations of blue tits (Cyanistes caeruleus, n = 31), great tits (Parus major, n = 35), and pied flycatchers (Ficedula hypoleuca, n = 20) across Europe, we assessed the influence of two local climatic variables (mean temperature and mean precipitation in February-May) on spatial synchrony in three fitness-related traits: laying date, clutch size, and fledgling number. We found a high degree of spatial synchrony in laying date but a lower degree in clutch size and fledgling number for each species. Temperature strongly influenced spatial synchrony in laying date for resident blue tits and great tits but not for migratory pied flycatchers. This is a relevant finding in the context of environmental impacts on populations because spatial synchrony in fitness-related trait values among populations may influence fluctuations in vital rates or population abundances. If environmentally induced spatial synchrony in fitness-related traits increases the spatial synchrony in vital rates or population abundances, this will ultimately increase the risk of extinction for populations and species. Assessing how environmental conditions influence spatiotemporal variation in trait values improves our mechanistic understanding of environmental impacts on populations.

Species-specific song responses emerge as a by-product of tuning to the local dialect.

Oscine birds preferentially respond to certain sounds over others from an early age, which focuses subsequent learning onto sexually relevant songs.1,2,3 Songs vary both across species and, due to cultural evolution, among populations of the same species. As a result, early song responses are expected to be shaped by selection both to avoid the fitness costs of cross-species learning4 and to promote learning of population-typical songs.5 These sources of selection are not mutually exclusive but can result in distinct geographic patterns of song responses in juvenile birds: if the risks of interspecific mating are the main driver of early song discrimination, then discrimination should be strongest where closely related species co-occur.4 In contrast, if early discrimination primarily facilitates learning local songs, then it should be tuned to songs typical of the local dialect.5,6,7 Here, we experimentally assess the drivers of song discrimination in nestling pied flycatchers (Ficedula hypoleuca). We first demonstrate that early discrimination against the songs of the closely related collared flycatcher (F. albicollis) is not strongly affected by co-occurrence. Second, across six European populations, we show that nestlings' early song responses are tuned to their local song dialect and that responses to the songs of collared flycatchers are similarly weak as to those of other conspecific dialects. Taken together, these findings provide clear experimental support for the hypothesis that cultural evolution, in conjunction with associated learning predispositions, drives the emergence of pre-mating reproductive barriers.

Phenotypic selection on an ornamental trait is not modulated by breeding density in a pied flycatcher population.

Most studies of phenotypic selection in the wild have focussed on morphological and life-history traits and looked at abiotic (climatic) variation as the main driver of selection. Consequently, our knowledge of the effects of biotic environmental variation on phenotypic selection on sexual traits is scarce. Population density can be considered a proxy for the intensity of intrasexual and intersexual competition and could therefore be a key factor influencing the covariation between individual fitness and the expression of sexual traits. Here, we used an individual-based data set from a population of pied flycatchers (Ficedula hypoleuca) monitored over 24 years to analyze the effect of breeding density on phenotypic selection on dorsal plumage colouration, a heritable and sexually selected ornament in males of this species. Using the number of recruits as a fitness proxy, our results showed overall stabilizing selection on male dorsal colouration, with intermediate phenotypes being favoured over extremely dark and dull individuals. However, our results did not support the hypothesis that breeding density mediates phenotypic selection on this sexual trait. We discuss the possible role of other biotic factors influencing selection on ornamental plumage.

High frequency of social polygyny reveals little costs for females in a songbird.

Mating system theory predicts that social polygyny-when one male forms pair bonds with two females-may evolve by female choice in species with biparental care. Females will accept a polygynous male if the benefit of mating with a male providing high-quality genes or rearing resources outweighs the cost of sharing mate assistance in parental care. Based on this rationale, we hypothesise that the population frequency of social polygyny (FSP) varies due to changes in mate sharing costs caused by changing environmental conditions. We predicted that: (1) polygamous females (i.e. mated with a polygynous male) pay a survival cost compared to monogamous females; (2) FSP would be higher in years with better rearing conditions and (3) the difference in survival rates between monogamous and polygamous females would be small following years with higher FSP. We tested these predictions using regression and multistate analyses of capture-recapture data of pied flycatchers, Ficedula hypoleuca, in central Spain collected over 26 years (1990-2016). Monogamous females had a higher mean survival rate than polygamous females (prediction 1), but there was no difference in survival between polygynous and monogamous males. In addition, FSP was positively associated with annual reproductive success (a proxy of the quality of rearing conditions-prediction 2). Finally, following years with high FSP, the survival of polygamous females was similar to that of monogamous females (prediction 3), while the chance of breeding in a polygamous state for 2 years in a row increased for both males and females. Our findings suggest that fluctuating environmental conditions may be a necessary but neglected aspect of understanding social polygyny mechanisms.

Population differences in the length and early-life dynamics of telomeres among European pied flycatchers.

Telomere length and shortening rate are increasingly being used as biomarkers for long-term costs in ecological and evolutionary studies because of their relationships with survival and fitness. Both early-life conditions and growth, and later-life stressors can create variation in telomere shortening rate. Studies on between-population telomere length and dynamics are scarce, despite the expectation that populations exposed to varying environmental constraints would present divergent telomere length patterns. The pied flycatcher (Ficedula hypoleuca) is a passerine bird breeding across Eurasia (from Spain to western Siberia) and migrating through the Iberian Peninsula to spend the nonbreeding period in sub-Saharan Africa. Thus, different populations show marked differences in migration distance. We studied the large-scale variation of telomere length and early-life dynamics in the pied flycatcher by comparing six European populations across a north-south gradient (Finland, Estonia, England and Spain) predicting a negative effect of migration distance on adult telomere length, and of nestling growth on nestling telomere dynamics. There were clear population differences in telomere length, with English birds from midlatitudes having the longest telomeres. Telomere length did not thus show consistent latitudinal variation and was not linearly linked to differences in migration distance. Early-life telomere shortening rate tended to vary between populations. Fast growth was associated with shorter telomeres in the early life, but faster nestling growth affected telomeres more negatively in northern than southern populations. While the sources of between-population differences in telomere-related biology remain to be more intensively studied, our study illustrates the need to expand telomere studies at the between-population level.

Fluctuating selection driven by global and local climatic conditions leads to stasis in breeding time in a migratory bird.

The origin of natural selection is linked to environmental heterogeneity, which influences variation in relative fitness among phenotypes. However, individuals in wild populations are exposed to a plethora of biotic and abiotic environmental factors. Surprisingly, the relative influence of multiple environmental conditions on the relative fitness of phenotypes has rarely been tested in wild populations. Identifying the main selection agent(s) is crucial when the target phenotype is tightly linked to reproduction and when temporal variation in selection is expected to affect evolutionary responses. By using individual-based data from a 29-year study of a short-lived migratory songbird, the pied flycatcher (Ficedula hypoleuca), we studied the relative influence of 28 temperature- and precipitation-based factors at local and global scales on selection on breeding time (egg laying) at the phenotypic level. Selection, estimated using the number of recruits as a proxy for fitness, penalized late breeders. Minimum temperatures in April and May were the environmental drivers that best explained selection on laying date. In particular, there was negative directional selection on laying date mediated by minimum temperature in April, being strongest in cold years. In addition, nonlinear selection on laying date was influenced by minimum temperatures in May, with selection on laying date changing from null to negative as the breeding season progressed. The intensity of selection on late breeders increased when minimum temperatures in May were highest. Our results illustrate the complex influence of environmental factors on selection on laying date in wild bird populations. Despite minimum temperature in April being the only variable that changed over time, its increase did not induce a shift in laying date in the population. In this songbird population, stabilizing selection has led to a three-decade stasis in breeding time. We suggest that variation in the effects of multiple climatic variables on selection may constrain phenotypic change.

Phenology-mediated effects of phenotype on the probability of social polygyny and its fitness consequences in a migratory passerine.

Why females engage in social polygyny remains an unresolved question in species where the resources provided by males maximize female fitness. In these systems, the ability of males to access several females, as well as the willingness of females to mate with an already mated male, and the benefits of this choice, may be constrained by the socio-ecological factors experienced at the local scale. Here, we used a 19-year dataset from an individual-monitored population of pied flycatchers (Ficedula hypoleuca) to establish local networks of breeding pairs. Then, we examined whether the probability of becoming socially polygynous and of mating with an already mated male (thus becoming a secondary female) is influenced by morphological and sexual traits as proxies of individual quality relative to the neighbours. We also evaluated whether social polygyny is adaptive for females by examining the effect of females' mating status (polygamously-mated vs monogamously-mated) on direct (number of recruits in a given season) and indirect (lifetime number of fledglings produced by these recruits) fitness benefits. The phenotypic quality of individuals, by influencing their breeding asynchrony relative to their neighbours, mediated the probability of being involved in a polygynous event. Individuals in middle-age (2-3 years), with large wings and, in the case of males, with conspicuous sexual traits, started to breed earlier than their neighbours. By breeding locally early, males increased their chances of becoming polygynous, while females reduced their chances of mating with an already mated male. Our results suggest that secondary females may compensate the fitness costs, if any, of sharing a mate, since their number of descendants did not differ from monogamous females. We emphasize the need of accounting for local breeding settings (ecological, social, spatial, and temporal) and the phenotypic composition of neighbours to understand individual mating decisions.

Providing longer post-fledging periods increases offspring survival at the expense of future fecundity.

The cost of reproduction is a key concept in life-history trade-offs. However, our understanding of the reproductive costs is biased towards measures of reproductive effort obtained before offspring independence. During the post-fledging dependence period (PFDP), it is well known that parents feed and protect their offspring. However, the effort devoted to this reproductive activity has never been considered in the context of of the costs of reproduction. Moreover, the potential fitness benefits and costs for offspring and parents, respectively, of the duration of the PFDP are largely unknown. We estimated the duration of the PFDP over 5 years using wild common kestrels (Falco tinnunculus) and studied its association with survival probability and future parental reproductive performance. Our results show that longer PFDPs increase the survival probability of fledglings, probably due to the benefits obtained from parental care. In addition, we found that providing longer PFDPs was associated with reduced clutch sizes but not the number of fledglings in the subsequent breeding season in males. We suggest that increased parental expenditures on offspring during the PFDP may represent a potential cost of reproduction in breeding males.

A negative association between bromadiolone exposure and nestling body condition in common kestrels: management implications for vole outbreaks.

BACKGROUND: Vole outbreaks have been extensively described, along with their impacts on humans, particularly in agricultural areas. The use of rodenticides is a common legal practice to minimise crop damage induced by high vole density for biocidal use. However, rodenticides can have negative direct and indirect impacts on non-target species that feed on voles. We studied whether the use of a second-generation anticoagulant rodenticide (SGAR), bromadiolone, can be detected in the blood of fledglings of wild common kestrels Falco tinnunculus in two areas of central Spain, exploring its possible indirect effects. RESULTS: We found that 16.9% of fledglings had a detectable concentration of bromadiolone in their blood, with an average concentration of 0.248 ± 0.023 ng mL-1 . Fledglings with bromadiolone in their blood, regardless of the concentration, had 6.7% lower body mass than those without detectable bromadiolone. CONCLUSION: The use of bromadiolone was detectable in the blood of alive non-target species. Detected bromadiolone in blood may reduce the body condition of nestlings, potentially reducing their fitness. The source of bromadiolone found in nestlings needs to be determined in future studies to derive accurate management advice. However, we urge the discontinuation of official SGAR distribution to farmers and their use in agrarian lands to minimise damage of voles on crops, particularly where common kestrels breed, and encourage the use of alternative effective practices. © 2016 Society of Chemical Industry.

Heritability of fear of humans in urban and rural populations of a bird species.

Flight initiation distance (FID), a measure of an animal's tolerance to human disturbance and a descriptor of its fear of humans, is increasingly employed for conservation purposes and to predict the response of species to urbanization. However, most work devoted to understanding variability in FID has been conducted at the population level and little is still known about inter-individual variability in this behaviour. We estimated the heritability of FID, a factor fundamental to understanding the strength and evolutionary consequences of selection of particular phenotypes associated with human disturbances. We used a population of burrowing owls (Athene cunicularia) monitored long-term and for which FID was previously shown to be highly consistent across an individual's lifespan. Heritability estimates varied between 0.37 and 0.80, depending on the habitat considered (urban-rural) and method used (parent-offspring regressions or animal models). These values are unusually high compared with those previously reported for other behavioural traits. Although more research is needed to fully understand the underlying causes of this resemblance between relatives, selection pressures acting on this behaviour should be seriously considered as an important evolutionary force in animal populations increasingly exposed to human disturbance worldwide.

Old males reduce melanin-pigmented traits and increase reproductive outcome under worse environmental conditions in common kestrels.

Secondary sexual traits displayed by males and females may have evolved as a signal of individual quality. However, both individual quality and investment on producing or maintaining enhanced sexual traits change as individuals age. At the same time, the costs associated to produce sexual traits might be attenuated or increased if environmental conditions are benign or worse respectively. Accordingly, environmental conditions are expected to shape the association between the expression of sexual traits and their reproductive outcome as individuals age. Nonetheless, little is known about the environmental influence on the co-variation between sexual traits and reproductive outcome throughout the life of individuals. We studied the age-dependency of the number and size of back spots, a melanin-based and sexual trait in adults of common kestrels (Falco tinnunculus). We analysed the age-dependence of reproductive traits and the environmental influence, defined as vole abundance, using a 10-year individual-based dataset. We broke down age-related changes of reproductive traits into within- and between-individual variation to assess their contribution to population-level patterns. Our results showed a within-individual decrease in the number, but not the size, of back spots in males. The size of back spots was positively correlated with food availability in males. Reproductive performance of males increased as they aged, in agreement with the life-history theory but depending of vole abundance. Remarkably, we found that having fewer back spots was positively associated with clutch size only for old individuals under low-food conditions. We suggest that environmental variation may shape the association between the expression of a sexual signal and reproductive outcome. We speculate that the reliability of sexual traits is higher when environmental conditions are poor only for old individuals. Within an evolutionary context, we suggest that the expression of sexual traits might be constrained by environmental conditions at later stages of life.

Insights into population ecology from long-term studies of red grouse Lagopus lagopus scoticus.

Long-term studies have been the backbone of population ecology. The red grouse Lagopus lagopus scoticus is one species that has contributed widely to this field since the 1950s. This paper reviews the trajectory and profound impact that these studies have had. Red grouse research has combined long-term studies of marked individuals with demographic studies over wide geographical areas and replicated individual- and population-level manipulations. A main focus has been on understanding the causes of population cycles in red grouse, and in particular the relative importance of intrinsic (behaviour) and extrinsic (climate, food limitation and parasite) mechanisms. Separate studies conducted in different regions initially proposed either the nematode parasite Trichostrongylus tenuis or changes in male aggressiveness in autumn as drivers of population cycles. More recent experiments suggest that parasites are not a necessary cause for cycles and have highlighted that behavioural and parasite-mediated mechanisms are interrelated. Long-term experiments show that parasites and aggressiveness interact. Two outstanding questions remain to be tested experimentally. First, what intrinsic mechanism causes temporal variation in patterns of male aggressiveness? The current favoured mechanism is related to patterns of kin structuring although there are alternative hypotheses. Second, how do the dual, interacting mechanisms, affect population dynamics? Red grouse studies have had an important impact on the field of population ecology, in particular through highlighting: (1) the impact of parasites on populations; (2) the role of intrinsic mechanisms in cyclic dynamics and (3) the need to consider multiple, interacting mechanisms.

Social context decouples the relationship between a sexual ornament and testosterone levels in a male wild bird.

In order to maximise fitness individuals should adjust their level of signalling according to their surrounding social environment. However, field experiments showing such adjustment of current signalling associated to changes in social context are lacking. Here, we manipulated levels of male aggressive- and dominance-related displays in a wild bird in our treated area by increasing testosterone levels using implants in a subset of males. We then compared the expression of sexual signals (i.e. comb size) between non-treated red grouse Lagopus lagopus scoticus males from control and treatment areas. We further explored the potential endocrinological mechanism linking social environment and signal expression by analysing testosterone levels in all males. Our treatment successfully increased overall aggressive- and dominance-related behaviours in the treatment area. Furthermore, testosterone-implanted birds increased their comb size as repeatedly shown in previous studies in male red grouse. Interestingly, untreated males living in the treatment area decreased their comb size, whilst increasing testosterone levels. Since comb size is a signal of dominance, untreated males from the treatment area may have perceived themselves as subordinate individuals and decreased their signalling levels to avoid confrontations with testosterone-treated, dominant individuals. In conclusion, our findings show that social context has the potential to regulate sexual signalling and testosterone levels. Our results highlight the role of social context when exploring the link between testosterone and behaviour, as it may reverse the relationship between both traits. Our results suggest that social context affects signalling and testosterone independently.

Parasitized mates increase infection risk for partners.

Individuals can gain fitness benefits and costs through their mates. However, studies on sexual selection have tended to focus on genetic benefits. A potentially widespread cost of pairing with a parasitized mate is that doing so will increase an individual's parasite abundance. Such a cost has been overlooked in systems in which parasites are indirectly transmitted. We manipulated the abundance of the nematode parasite Trichostrongylus tenuis, an indirectly transmitted parasite, within pairs of wild red grouse Lagopus lagopus scoticus in spring. Parasite levels were correlated within pairs before the experiment. We removed parasites from males, females, or both members of the pair and evaluated individual parasite uptake over the subsequent breeding period. At the end of the breeding season, an individual's parasite abundance was greater when its mate had not been initially purged of parasites. This cost appeared to be greater for males. We discuss the implications of our results in relation to the costs that parasites may have on sexual selection processes.

The ornament-condition relationship varies with parasite abundance at population level in a female bird.

Environmental heterogeneity is expected to create variation in the ornament-condition relationship. This topic has been studied in males with less attention being given to females. Here, we explore inter-population variation in the relationship between the size of a male-like trait, supra-orbital combs, and body mass in female red grouse Lagopus lagopus scoticus. We used the abundance of the nematode Trichostrongylus tenuis, a parasite with strong negative effects on this species, as a proxy of environmental conditions. We studied six populations over 5 years and showed that the comb size-body mass relationship varied with mean parasite abundance, with stronger ornament-condition relationships in populations with higher parasite infection levels. Our study supports the idea that environmental conditions, and in particular parasite infection levels, may affect the reliability of female ornaments as condition indicators.

Does egg colouration reflect male condition in birds?

How colouration provides information about individuals in birds has been a central issue in recent decades. Although much information has been derived, little is known about the adaptive significance of egg colouration in birds. A recent idea suggests that biliverdin- and porphyrin-pigmented eggs may act as a post-mating sexual signal for males to assess female quality. In birds, it is common for males to influence prelaying female condition by courtship feeding. Using Eurasian kestrels, a species that lays protoporphyrin-pigmented eggs, we descriptively assessed the influence of male feeding on egg pigmentation by considering female phenotype, condition, breeding parameters and male body condition. We found that older females and females with greyer tails (an index of individual quality) produce highly pigmented eggs. However, male body condition was the only variable that explained egg colouration when considered together with the female-related variables. Therefore, females that mated with males in better condition laid highly pigmented eggs. With the same species, we also explored the cost of producing protoporphyrin-pigmented eggs using a food-supply experiment before the laying period. Food supplementation did not increase egg pigmentation, but hatching success and egg mass were positively related to egg colouration only in food supplied pairs. We suggest that egg colouration might be costly to produce and probably suggests egg quality. However, this cost cannot be explained by female quality, but by male condition instead. In general, our results do not support the theory that egg colouration is a post-mating sexual signal in species where males determine female condition at the time of laying.