RESUMEN
Colonization of a novel environment by a few individuals can lead to rapid evolutionary change, yet there is scarce evidence of the relative contributions of neutral and selective factors in promoting divergence during the early stages of colonization. Here we explore the role of neutral and selective forces in the divergence of a unique urban population of the dark-eyed junco (Junco hyemalis), which became established on the campus of the University of California at San Diego (UCSD) in the early 1980s. Previous studies based on microsatellite loci documented significant genetic differentiation of the urban population as well as divergence in phenotypic traits relative to nearby montane populations, yet the geographical origin of the colonization and the contributing factors remained uncertain. Our genome-wide single nucleotide polymorphism data set confirmed the marked genetic differentiation of the UCSD population, and we identified the coastal subspecies pinosus from central California as its sister group instead of the neighbouring mountain population. Demographic inference recovered a separation from pinosus as recent as 20-32 generations ago after a strong bottleneck, suggesting a role for drift in genetic differentiation. However, we also found significant associations between habitat variables and genome-wide variants linked to functional genes, some of which have been reported as potentially adaptive in birds inhabiting modified environments. These results suggest that the interplay between founder events and selection may result in rapid shifts in neutral and adaptive loci across the genome, and reveal the UCSD junco population as a case of contemporary evolutionary divergence in an anthropogenic environment.
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Passeriformes , Pájaros Cantores , Animales , Evolución Biológica , Flujo Genético , Genética de Población , Fenotipo , Pájaros Cantores/genéticaRESUMEN
Allochrony, the mismatch of reproductive schedules, is one mechanism that can mediate sympatric speciation and diversification. In songbirds, the transition into breeding condition and gonadal growth is regulated by the hypothalamic-pituitary-gonadal (HPG) axis at multiple levels. We investigated whether the difference in reproductive timing between two seasonally sympatric subspecies of dark-eyed juncos (Junco hyemalis) was related to gene expression along the HPG axis. During the sympatric pre-breeding stage, we measured hypothalamic and testicular mRNA expression of candidate genes via qPCR in captive male juncos. For hypothalamic mRNA, we found our earlier breeding subspecies had increased expression of gonadotropin-releasing hormone (GnRH) and decreased expression of androgen receptor, oestrogen receptor alpha and mineralocorticoid receptor (MR). Subspecies did not differ in expression of hypothalamic gonadotropin-inhibitory hormone (GnIH) and glucocorticoid receptor (GR). While our earlier breeding subspecies had higher mRNA expression of testicular GR, subspecies did not differ in testicular luteinizing hormone receptor, follicle-stimulating hormone receptor or MR mRNA expression levels. Our findings indicate increased GnRH production and decreased hypothalamic sensitivity to sex steroid negative feedback as factors promoting differences in the timing of gonadal recrudescence between recently diverged populations. Differential gene expression along the HPG axis may facilitate species diversification under seasonal sympatry.
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Proteínas Aviares/genética , Expresión Génica , Hipotálamo/metabolismo , Reproducción/fisiología , Pájaros Cantores/genética , Testículo/metabolismo , Animales , Proteínas Aviares/metabolismo , Masculino , ARN Mensajero/genética , ARN Mensajero/metabolismo , Reproducción/genética , Estaciones del Año , Pájaros Cantores/crecimiento & desarrollo , SimpatríaRESUMEN
Reproductive allochrony presents a potential barrier to gene flow and is common in seasonally sympatric migratory and sedentary birds. Mechanisms mediating reproductive allochrony can influence population divergence and the capacity of populations to respond to environmental change. We asked whether reproductive allochrony in seasonally sympatric birds results from a difference in response to supplementary or photoperiodic cues and whether the response varies in relation to the distance separating breeding and wintering locations as measured by stable isotopes. We held seasonally sympatric migratory and sedentary male dark-eyed juncos (Junco hyemalis) in a common garden in early spring under simulated natural changes in photoperiod and made measurements of reproductive and migratory physiology. On the same dates and photoperiods, sedentary juncos had higher testosterone (initial and gonadotropin-releasing hormone induced), more developed cloacal protuberances, and larger testes than migrants. In contrast, migratory juncos had larger fat reserves (fuel for migration). We found a negative relationship between testis mass and feather hydrogen isotope ratios, indicating that testis growth was more delayed in migrants making longer migrations. We conclude that reproductive allochrony in seasonally sympatric migratory and sedentary birds can result from a differential response to photoperiodic cues in a common garden, and as a result, gene flow between migrants and residents may be reduced by photoperiodic control of reproductive development. Further, earlier breeding in response to future climate change may currently be constrained by differential response to photoperiodic cues.
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Migración Animal/fisiología , Passeriformes/fisiología , Fotoperiodo , Simpatría , Tejido Adiposo , Animales , Cambio Climático , Deuterio/análisis , Plumas/química , Hormona Liberadora de Gonadotropina/farmacología , Masculino , Tamaño de los Órganos , Estaciones del Año , Testículo/crecimiento & desarrollo , Testosterona/sangreRESUMEN
Sexual signals contain information on individual quality or motivation, and most explanations for their reliability are based on signal costs. A recent suggestion is that signaling mistakes, defined as deviations from typical signal design, provide cues on individual quality, contributing to reliable communication even when signal design is not costly. We describe several atypical song traits in dark-eyed juncos (Junco hyemalis) that may be mistakes during song production or development and occur in up to 6% of songs. These putative mistakes were more frequent in an urban versus a wildland population, and individuals differed in their frequency of mistakes. Some atypical signals were more frequent in younger males or were negatively related to paternity success, supporting the hypothesis that fewer mistakes indicate individual quality. We also discuss unexpected results, such as some atypical signals being more frequent in more ornamented males and in songs with lower performance demands. Song consistency (similarity across syllable renditions) was positively related to male age and paternity success; nonetheless, relations with paternity were stronger when looking at the most deviant syllable renditions, suggesting that the perceptual salience of large mistakes may mediate receiver responses to song consistency. Results indicate that signaling mistakes reveal relevant information to play a role in communication.
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Passeriformes/fisiología , Conducta Sexual Animal/fisiología , Vocalización Animal/fisiología , Factores de Edad , Comunicación Animal , Animales , California , Ecosistema , Fertilidad/fisiología , MasculinoRESUMEN
In an era of climate change, understanding the genetic and physiological mechanisms underlying flexibility in phenology and life history has gained greater importance. These mechanisms can be elucidated by comparing closely related populations that differ in key behavioural and physiological traits such as migration and timing of reproduction. We compared gene expression in two recently diverged dark-eyed Junco (âJunco hyemalis) subspecies that live in seasonal sympatry during winter and early spring, but that differ in behaviour and physiology, despite exposure to identical environmental cues. We identified 547 genes differentially expressed in blood and pectoral muscle. Genes involved in lipid transport and metabolism were highly expressed in migrant juncos, while genes involved in reproductive processes were highly expressed in resident breeders. Seasonal differences in gene expression in closely related populations residing in the same environment provide significant insights into mechanisms underlying variation in phenology and life history, and have potential implications for the role of seasonal timing differences in gene flow and reproductive isolation.
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Migración Animal , Regulación de la Expresión Génica , Músculos Pectorales/química , Reproducción , Estaciones del Año , Pájaros Cantores/clasificación , Pájaros Cantores/fisiología , Transcriptoma , Animales , Proteínas Aviares/genética , Proteínas Aviares/metabolismo , Análisis Químico de la Sangre/veterinaria , Masculino , Pájaros Cantores/genética , Especificidad de la Especie , Simpatría , VirginiaRESUMEN
To optimally time reproduction, animals must coordinate changes in the hypothalamo-pituitary-gonadal (HPG) axis. The extent of intra-species variation in seasonal timing of reproductive function is considerable, both within and among populations. Dark-eyed junco (Junco hyemalis) populations are known to differ in their reproductive timing response to cues experienced in the same habitat in late winter/early spring. Specifically in juncos cohabitating on shared wintering grounds, residents initiate breeding and reproductive activity but migrants delay reproductive development and prepare to migrate before breeding. Here, we test the hypothesis that the pituitary gland acts as a 'control point' to modulate differential HPG axis activity across populations. We sampled free-living resident and migrant juncos on their shared over-wintering grounds in March, thus all individuals were experiencing the same environmental cues, including photoperiod. We predicted that during this critical time of transition, residents would more readily respond to repeated gonadotropin releasing hormone (GnRH) stimulation with increases in luteinizing hormone (LH), in contrast to migrants, which should delay full reproductive activity. Our data indicate that migrant females, while still on the overwintering grounds, have a reduced LH response to repeated GnRH injections compared to resident females. Male migrant and resident birds did not differ in their responsiveness to repeated GnRH. Our results suggest a sex difference in the costs of mistimed activation of the HPG axis, with female migrants being less responsive than residents females and males to repeated stimulation. Further, our data implicate a key role for the pituitary in regulating appropriate reproductive timing responses.
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Hormona Liberadora de Gonadotropina/metabolismo , Hormona Luteinizante/metabolismo , Caracteres Sexuales , Animales , Cruzamiento , Femenino , Masculino , Pájaros CantoresRESUMEN
Climate change, habitat alteration, range expansions, and biological invasions are all predicted to require rapid shifts in multiple traits including behavior and life history, both for initial population establishment and subsequent adaptation. Hormonal mechanisms likely play a key role in facilitating or constraining plastic and genetic responses for suites of traits, but few studies have evaluated their role in shaping contemporary adaptation or diversification. We examined multiple phenotypic adjustments and associated hormonal changes following a recent (early 1980s) colonization event, in which a temperate-breeding songbird, the dark-eyed junco (Junco hyemalis), became established in the Mediterranean climate of San Diego, California. The milder climate has led to an extended breeding season and year-round residency, and we document shifts in multiple sexually selected behaviors and plumage traits. Testosterone titers in San Diego were elevated for longer but with a lower peak value compared to a nearby native-range population, and correlations between testosterone and related traits were similar within and among populations. A common garden study indicated that changes in testosterone likely represent plastic responses to the less seasonal environment of the city, providing the context against which subsequent genetic changes in morphology likely occurred. We argue that correlated shifts in multiple traits, organized by underlying physiology, may be a generally important element of many successful adjustments to changing environments.
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Adaptación Fisiológica , Ecosistema , Passeriformes/fisiología , Pigmentación/fisiología , Conducta Sexual Animal , Testosterona/sangre , Animales , California , Ciudades , Clima , Femenino , Masculino , Fenotipo , Reproducción , Estaciones del AñoRESUMEN
American robins and dark-eyed juncos migrate across North America and have been found to be competent hosts for some bacterial and viral pathogens, but their contributions to arthropod-borne diseases more broadly remain poorly characterized. Here, we sampled robins and juncos in multiple sites across North America for arthropod-borne bacterial pathogens of public health significance. We identified two novel Rickettsia spp. in one wintering migrant per bird species related to bellii, transitional, and spotted rickettsiae fever groups. Stable isotope analyses of feathers suggested spring migration of these common songbirds could disperse these novel rickettsiae hundreds-to-thousands of kilometers to host breeding grounds. Further work is needed to characterize zoonotic potential of these rickettsiae and host reservoir competence.
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Rickettsia , Pájaros Cantores , Animales , Rickettsia/genética , Estaciones del Año , América del NorteRESUMEN
Environmental changes caused by urbanization and noise pollution can have profound effects on acoustic communication. Many organisms use higher sound frequencies in urban environments with low-frequency noise, but the developmental and evolutionary mechanisms underlying these shifts are generally unknown. We used a common garden experiment to ask whether changes in minimum song frequency observed 30 years after a songbird colonized an urban environment are a consequence of behavioural flexibility. We captured male juvenile dark-eyed juncos, Junco hyemalis thurberi, from two populations (urban and mountain) soon after they reached independence (aged 25-40 days), raised them in identical indoor aviaries and studied their songs at an age of 3 years. We found that the large population difference in minimum frequency observed in the field persisted undiminished in the common garden despite the absence of noise. We also found some song sharing between the common garden and natal field populations, indicating that early song memorization before capture could contribute to the persistent song differences in adulthood. These results are the first to show that frequency shifts in urban birdsong are maintained in the absence of noise by genetic evolution and/or early life experiences.
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Long-distance migrations influence the physiology, behavior, and fitness of migratory animals throughout their annual cycles, and fundamentally alter their interactions with parasites. Several hypotheses relating migratory behavior to the likelihood of parasitism have entered the literature, making conflicting, testable predictions. To assess how migratory behavior of hosts is associated with parasitism, we compared haemosporidian parasite infections between two closely related populations of a common North American sparrow, the dark-eyed junco, that co-occur in shared habitats during the non-breeding season. One population is sedentary and winters and breeds in the Appalachian Mountains. The other population is migratory and is found in seasonal sympatry with the sedentary population from October through April, but then flies (≥ 900 km) northwards to breed. The populations were sampled in the wild on the shared montane habitat at the beginning of winter and again after confining them in a captive common environment until the spring. We found significantly higher prevalence of haemosporidian parasite infections in the sedentary population. Among infected juncos, we found no difference in parasite densities (parasitemias) between the sedentary and migrant populations and no evidence for winter dormancy of the parasites. Our results suggest that long-distance migration may reduce the prevalence of parasite infections at the population level. Our results are inconsistent with the migratory exposure hypothesis, which posits that long-distance migration increases exposure of hosts to diverse parasites, and with the migratory susceptibility hypothesis, which posits that trade-offs between immune function and migration increase host susceptibility to parasites. However, our results are consistent with the migratory culling hypothesis, which posits that heavily infected animals are less likely to survive long-distance migration, and with the migratory escape hypothesis, which posits that long-distance migration allows host populations to seasonally escape areas of high infection risk.
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Migración Animal/fisiología , Haemosporida/patogenicidad , Infecciones Protozoarias en Animales/epidemiología , Pájaros Cantores/fisiología , Animales , Prevalencia , Estaciones del Año , Conducta Sedentaria , Pájaros Cantores/parasitología , SimpatríaRESUMEN
Social learning enables the adjustment of behaviour to complex social and ecological tasks, and underlies cultural traditions. Understanding when animals use social learning versus other forms of behavioural development can help explain the dynamics of animal culture. The dark-eyed junco (Junco hyemalis) is a songbird with weak cultural song traditions because, in addition to learning songs socially, male juncos also invent or improvise novel songs. We compared songs shared by multiple males (i.e. socially learned) with songs recorded from only one male in the population (many of which should be novel) to gain insight into the advantages of social learning versus invention or improvisation. Song types shared by multiple males were on average of lower performance, on aspects of vocal performance that have been implicated in agonistic communication in several species. This was not explained by cultural selection among socially learned songs (e.g. selective learning) because, for shared song types, song performance did not predict how many males shared them. We discuss why social learning does not maximize song performance in juncos, and suggest that some songbirds may add novel songs to culturally inherited repertoires as a means to acquire higher-quality signals.
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Recent studies exploring the molecular genetic basis for migratory variation in animals have identified polymorphisms in two genes ( CLOCK and ADCYAP1) that are linked to circadian rhythms and correlate with migratory propensity and phenology among individuals and populations. Results from these initial studies are mixed, however, and additional data are needed to assess the generality and diversity of the molecular mechanisms that regulate the biology of migration. We sequenced CLOCK and ADCYAP1 in 15 populations across the two species of the avian genus Junco, a North American lineage in which multiple recently diverged subspecies and populations range from sedentary to long-distance migrants. We found no consistent associations between allele length and migratory status across the genus for either CLOCK or ADCYAP1. However, within two subspecies groups, populations that migrate longer distances have longer CLOCK alleles on average. Additionally, there was a positive relationship between ADCYAP1 allele length and migratory restlessness (zugunruhe) among individuals within one of two captive populations studied-a result similar to those reported previously within captive blackcaps ( Sylvia atricapilla). We conclude that, while both ADCYAP1 and CLOCK may correlate with migratory propensity within or among certain populations or species, previously identified relationships between migratory behavior and sequence variants cannot be easily generalized across taxa.
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Demanding performance of vocal signals, such as birdsong, may be evaluated by trade-offs among acoustic traits. If individuals differ in their ability to sustain physiologically demanding singing, then aspects of song performance resulting from such trade-offs could signal individual quality. Song performance can also differ among song types, and it is not known whether this influences the assessment of individual quality. We asked whether three trade-off-based measures of song performance indicate male age or aspects of condition (body condition, hematocrit and ectoparasite load) in the dark-eyed junco (Junco hyemalis), a species with small repertoires. Across a sample of over 100 males, no measure of song performance was related to male age or condition, nor did song performance improve with age for those males recorded in consecutive years. In all cases, the variation in song performance explained by these predictors was small (<4%). Instead, the more song types we recorded from a male, the more likely we were to record high-performance songs, and this sampling effect was stronger than putative correlations with male quality. These results complement a previous study on this population showing that most variation in performance is found among song types rather than among males. Collectively, the lack of association between trade-off-based aspects of song performance and male age or condition, plus variation among song types that interferes with rapid assessment of a male's best performance, indicate that these aspects of song performance do not allow a good assessment of male quality in juncos, and perhaps more generally in species with song repertoires.
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We examined variation at MHC Class IIB genes in a recently established population of dark-eyed juncos (Junco hyemalis) in a coastal urban environment in southern California, USA relative to an ancestral-range population from a nearby species-typical montane environment. The founding population is estimated to have been quite small, but we predicted that variation at the major histocompatibility complex (MHC) among the founders would nevertheless be preserved owing to the high functional significance of MHC. Previous studies of MHC in songbirds have had varying degrees of success in isolating loci, as passerines show extensive MHC gene duplication. In order to compare diversity in the two populations, we employed two published approaches to sequencing MHC Class II exon 2: direct sequencing with exon-based primers, and traditional cloning and sequencing with intron-based primers. Results from both methods show that the colonist population has maintained high levels of variation. Our results also indicate varying numbers of alleles across individuals, corroborating evidence for gene duplication in songbird MHC. While future studies in songbirds may need to take a genomic approach to fully understand the structure of MHC in this lineage, our results show that it is possible to use traditional methods to reveal functional variation across populations.
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Novel or changing environments expose animals to diverse stressors that likely require coordinated hormonal and behavioral adaptations. Predicted adaptations to urban environments include attenuated physiological responses to stressors and bolder exploratory behaviors, but few studies to date have evaluated the impact of urban life on codivergence of these hormonal and behavioral traits in natural systems. Here, we demonstrate rapid adaptive shifts in both stress physiology and correlated boldness behaviors in a songbird, the dark-eyed junco, following its colonization of a novel urban environment. We compared elevation in corticosterone (CORT) in response to handling and flight initiation distances in birds from a recently established urban population in San Diego, California to birds from a nearby wildland population in the species' ancestral montane breeding range. We also measured CORT and exploratory behavior in birds raised from early life in a captive common garden study. We found persistent population differences for both reduced CORT responses and bolder exploratory behavior in birds from the colonist population, as well as significant negative covariation between maximum CORT and exploratory behavior. Although early developmental effects cannot be ruled out, these results suggest contemporary adaptive evolution of correlated hormonal and behavioral traits associated with colonization of an urban habitat.
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Evolutionary approaches to culture remain contentious. A source of contention is that cultural mutation may be substantial and, if it drives cultural change, then current evolutionary models are not adequate. But we lack studies quantifying the contribution of mutations to directional cultural change. We estimated the contribution of one type of cultural mutations--modification of memes--to directional cultural change using an amenable study system: learned birdsongs in a species that recently entered an urban habitat. Many songbirds have higher minimum song frequency in cities, to alleviate masking by low-frequency noise. We estimated that the input of meme modifications in an urban songbird population explains about half the extent of the population divergence in song frequency. This contribution of cultural mutations is large, but insufficient to explain the entire population divergence. The remaining divergence is due to selection of memes or creation of new memes. We conclude that the input of cultural mutations can be quantitatively important, unlike in genetic evolution, and that it operates together with other mechanisms of cultural evolution. For this and other traits, in which the input of cultural mutations might be important, quantitative studies of cultural mutation are necessary to calibrate realistic models of cultural evolution.
Asunto(s)
Pájaros Cantores/fisiología , Animales , California , Ambiente , Aprendizaje , Masculino , Ruido , Especificidad de la Especie , Vocalización AnimalRESUMEN
Songbirds often sing at higher frequency (pitch) in urban, noise-polluted areas, which reduces acoustic masking by low-frequency anthropogenic noise. Such frequency shifts, however, are less efficient at overcoming background noise than simply singing louder. Therefore, it was suggested that high-frequency singing might not be a functional adjustment to noise, but a physiological consequence of singing louder (also known as the Lombard effect). We tested for the first time the main tenet of this hypothesis, for birdsong whether increasing sound amplitude has a concomitant effect on song frequency, using a representative species with higher urban minimum frequency, the dark-eyed junco, Junco hyemalis. The frequency bandwidth of songs and syllables increased with amplitude, involving lower minimum frequency in louder songs and syllables. Therefore, louder singing does not explain the higher minimum frequency of urban dark-eyed juncos. Amplitude and peak frequency were weakly positively related across but not within songs, suggesting that increased frequency is not an obligatory outcome of singing louder. Instead, birds may adjust both amplitude and frequency in response to changing noise or motivation across songs. Our results suggest that adjustments in song frequency and amplitude are largely independent and, thus, can be complementary rather than alternative vocal adjustments to noise. We discuss oscine vocal physiology and details of the behaviour of urban birds, both of which we argue are consistent with the increased frequency of urban birdsong generally being a functional adjustment to noise, rather than a consequence of singing louder.
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Migratory animals provide unique spectacles of cultural, ecological, and economic importance. However, the process of migration is a source of risk for migratory species as human actions increasingly destroy and fragment habitat, create obstacles to migration, and increase mortality along the migration corridor. As a result, many migratory species are declining in numbers. In the United States, the Endangered Species Act provides some protection against extinction for such species, but no protection until numbers are severely reduced, and no guarantee of recovery to population levels associated with cultural, ecological, or economic significance. Although groups of species receive some protection from statutes such as the Migratory Bird Treaty Act and Marine Mammal Protection Act, there is no coordinated system for conservation of migratory species. In addition, information needed to protect migratory species is often lacking, limiting options for land and wildlife managers who seek to support these species. In this Article, we outline the existing scientific, legal, and management information and approaches to migratory species. Our objective is to assess present capacity to protect the species and the phenomenon of migration, and we argue that al three disciplines are necessary for effective conservation. We find significant capacity to support conservation in all three disciplines, but no organization around conservation of migration within any discipline or among the three disciplines. Areas of synergy exist among the disciplines but not as a result of any attempt for coordination. As a result, significant gaps in information and capacity exist that must be addressed if effective conservation of migratory species is to be undertaken. We suggest that all three disciplines cooperate to identify the most pressing research needs, so that these can become targets for relevant funding sources. We identify areas of current risk to migratory species that represent gaps in current legal protections: protective legislation that provides no guidelines for desirable population sizes or best management practices for migratory species, taxonomic groups, particularly those including long-distance migrants, for which no agency has oversight, and gaps in policies to address impacts of fragmentation and obstacles such as power lines and wind turbines that curtail migration or cause mortality. Finally, we suggest that state-level programs provide either a foundation to augment with, or a model on which to build, conservation efforts targeting migratory species. Problems will arise due to lack of funds, difficulties in securing a landscape that will support abundant migrations, lack of adequate standards and best management practices, and an insufficient culture of collaboration among the three main relevant disciplines. However, we view these problems as entirely soluble and see evidence of support in society at large for conservation of migratory species.
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Identifying important "migratory species" and the characteristics of their migrations might sound like a simple starting point for efforts to conserve and protect animal migrations. However, migrations are dynamic phenomena that vary over space and time, and migratory behaviors can vary substantially among closely related species, subspecies, races, or populations, and even among individual animals within a single population. The migratory behaviors of populations or individuals can also change rapidly-or be lost entirely-in response to habitat alteration or climate change. These complexities present both challenges and opportunities for initiatives to conserve animal migrations. In this Article, we discuss the concepts of intra-species variation in migration and the sensitivity of migrations to environmental change, and we consider the implications of these topics for legal, policy, management, and research agendas.
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Chemical signaling has been documented in many animals, but its potential importance in avian species, particularly songbirds, has received far less attention. We tested whether volatile compounds in the preen oil of a songbird (Junco hyemalis) contain reliable information about individual identity, sex, or population of origin by repeated sampling from captive male and female juncos originating from 2 recently diverged junco populations in southern California. One of the populations recently colonized an urban environment; the other resides in a species-typical montane environment. The birds were field-caught as juveniles, housed under identical conditions, and fed the same diet for 10 months prior to sampling. We used capillary gas chromatography-mass spectrometry to quantify the relative abundance of 19 volatile compounds previously shown to vary seasonally in this species. We found individual repeatability as well as significant sex and population differences in volatile profiles. The persistence of population differences in a common environment suggests that preen oil chemistry likely has a genetic basis and may thus evolve rapidly in response to environmental change. These finding suggest that songbird preen oil odors have the potential to function as chemosignals associated with mate recognition or reproductive isolation.