RESUMEN
In animals, reproductive performance typically improves over time early in life. Several ultimate and proximate mechanisms may contribute to such an age-related improvement and these mechanisms can act in a relative or in an absolute sense. Low performance of young individuals may be the consequence of a comparison or competition with older individuals (relative), or it may be due to specific traits of young individuals and be unrelated to the presence of older competitors (absolute). Here, we perform a test to disentangle whether the effect of age class (yearling or older) on male extra-pair siring success is relative or absolute. Male age is the most consistent predictor of male extra-pair siring success across bird species, yet the mechanisms underlying this pattern are not well understood. Low extra-pair siring success of yearling males may be a consequence of the presence of older ("adult") males (hypothesis 1), because adult males are more successful in intra- and intersexual interactions or because females prefer to copulate with adult males when available (relative preference). Alternatively, low extra-pair siring success of yearlings may be independent of the presence of adult males (hypothesis 2), for example, if yearling males on average invest less in extra-pair behavior or if females avoid them as extra-pair mates, independent of the availability of older males (absolute preference). To distinguish between these 2 hypotheses, we experimentally manipulated the age structure of a nest-box-breeding population of blue tits (Cyanistes caeruleus) by removing almost all adult males, and compared patterns of extra-pair paternity in the experimental year with those from the preceding 15 "control" years. Removal of adult males resulted in a substantial increase in the extra-pair siring success of yearling males compared to the "control" years, but did not affect the population-level frequency of extra-pair paternity or its spatial patterns. Our results provide clear evidence that extra-pair siring success of yearlings can increase and that it depends on the presence of older males in the population, indicating a relative effect of age on reproductive performance. These results suggest that older males outcompete yearling males in direct or indirect interactions, in sperm competition or as a result of differences in attractiveness to females.
Asunto(s)
Conducta Sexual Animal , Pájaros Cantores , Humanos , Animales , Femenino , Masculino , Semen , Reproducción , CruzamientoRESUMEN
The development of individuality during learned behavior is a common trait observed across animal species; however, the underlying biological mechanisms remain understood. Similar to human speech, songbirds develop individually unique songs with species-specific traits through vocal learning. In this study, we investigate the developmental and molecular mechanisms underlying individuality in vocal learning by utilizing F1 hybrid songbirds (Taeniopygia guttata cross with Taeniopygia bichenovii), taking an integrating approach combining experimentally controlled systematic song tutoring, unbiased discriminant analysis of song features, and single-cell transcriptomics. When tutoring with songs from both parental species, F1 hybrid individuals exhibit evident diversity in their acquired songs. Approximately 30% of F1 hybrids selectively learn either song of the two parental species, while others develop merged songs that combine traits from both species. Vocal acoustic biases during vocal babbling initially appear as individual differences in songs among F1 juveniles and are maintained through the sensitive period of song vocal learning. These vocal acoustic biases emerge independently of the initial auditory experience of hearing the biological father's and passive tutored songs. We identify individual differences in transcriptional signatures in a subset of cell types, including the glutamatergic neurons projecting from the cortical vocal output nucleus to the hypoglossal nuclei, which are associated with variations of vocal acoustic features. These findings suggest that a genetically predisposed vocal motor bias serves as the initial origin of individual variation in vocal learning, influencing learning constraints and preferences.
Asunto(s)
Individualidad , Pájaros Cantores , Animales , Humanos , Predisposición Genética a la Enfermedad , Habla , Acústica , SesgoRESUMEN
Seasonal migration is a widespread behavior relevant for adaptation and speciation, yet knowledge of its genetic basis is limited. We leveraged advances in tracking and sequencing technologies to bridge this gap in a well-characterized hybrid zone between songbirds that differ in migratory behavior. Migration requires the coordinated action of many traits, including orientation, timing, and wing morphology. We used genetic mapping to show these traits are highly heritable and genetically correlated, explaining how migration has evolved so rapidly in the past and suggesting future responses to climate change may be possible. Many of these traits mapped to the same genomic regions and small structural variants indicating the same, or tightly linked, genes underlie them. Analyses integrating transcriptomic data indicate cholinergic receptors could control multiple traits. Furthermore, analyses integrating genomic differentiation further suggested genes underlying migratory traits help maintain reproductive isolation in this hybrid zone.
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Migración Animal , Estaciones del Año , Pájaros Cantores , Animales , Migración Animal/fisiología , Pájaros Cantores/genética , Pájaros Cantores/fisiología , Especiación Genética , Hibridación Genética , Receptores Colinérgicos/genética , Receptores Colinérgicos/metabolismo , Genómica/métodos , Mapeo CromosómicoRESUMEN
Predicting how the range dynamics of migratory species will respond to climate change requires a mechanistic understanding of the factors that operate across the annual cycle to control the distribution and abundance of a species. Here, we use multiple lines of evidence to reveal that environmental conditions during the nonbreeding season influence range dynamics across the life cycle of a migratory songbird, the American redstart (Setophaga ruticilla). Using long-term data from the nonbreeding grounds and breeding origins estimated from stable hydrogen isotopes in tail feathers, we found that the relationship between annual survival and migration distance is mediated by precipitation, but only during dry years. A long-term drying trend throughout the Caribbean is associated with higher mortality for individuals from the northern portion of the species' breeding range, resulting in an approximate 500 km southward shift in breeding origins of this Jamaican population over the past 30 y. This shift in connectivity is mirrored by changes in the redstart's breeding distribution and abundance. These results demonstrate that the climatic effects on demographic processes originating during the tropical nonbreeding season are actively shaping range dynamics in a migratory bird.
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Passeriformes , Pájaros Cantores , Animales , Migración Animal , Región del Caribe , Dinámica Poblacional , Estaciones del AñoRESUMEN
Aggression is a crucial behavior that impacts access to limited resources in different environmental contexts. Androgens synthesized by the gonads promote aggression during the breeding season. However, aggression can be expressed during the non-breeding season, despite low androgen synthesis by the gonads. The brain can also synthesize steroids ("neurosteroids"), including androgens, which might promote aggression during the non-breeding season. Male song sparrows, Melospiza melodia, are territorial year-round and allow the study of seasonal changes in the steroid modulation of aggression. Here, we quantified steroids following a simulated territorial intrusion (STI) for 10â min in wild adult male song sparrows during the breeding and non-breeding seasons. Using liquid chromatography-tandem mass spectrometry (LC-MS/MS), we examined 11 steroids: pregnenolone, progesterone, corticosterone, dehydroepiandrosterone, androstenedione, testosterone, 5α-dihydrotestosterone, 17ß-estradiol, 17α-estradiol, estriol, and estrone. Steroids were measured in blood and 10 microdissected brain regions that regulate social behavior. In both seasons, STI increased corticosterone in the blood and brain. In the breeding season, STI had no rapid effects on androgens or estrogens. Intriguingly, in the non-breeding season, STI increased testosterone and androstenedione in several behaviorally relevant regions, but not in the blood, where androgens remained non-detectable. Also in the non-breeding season, STI increased progesterone in the blood and specific brain regions. Overall, rapid socially modulated changes in brain steroid levels are more prominent during the non-breeding season. Brain steroid levels vary with season and social context in a region-specific manner and suggest a role for neuroandrogens in aggression during the non-breeding season.
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Agresión , Andrógenos , Encéfalo , Estaciones del Año , Gorriones , Territorialidad , Animales , Masculino , Agresión/fisiología , Andrógenos/metabolismo , Encéfalo/metabolismo , Gorriones/fisiología , Gorriones/metabolismo , Pájaros Cantores/metabolismoRESUMEN
Island organisms often evolve phenotypes divergent from their mainland counterparts, providing a useful system for studying adaptation under differential selection. In the white-winged fairywren (Malurus leucopterus), subspecies on two islands have a black nuptial plumage whereas the subspecies on the Australian mainland has a blue nuptial plumage. The black subspecies have a feather nanostructure that could in principle produce a blue structural color, suggesting a blue ancestor. An earlier study proposed independent evolution of melanism on the islands based on the history of subspecies divergence. However, the genetic basis of melanism and the origin of color differentiation in this group are still unknown. Here, we used whole-genome resequencing to investigate the genetic basis of melanism by comparing the blue and black M. leucopterus subspecies to identify highly divergent genomic regions. We identified a well-known pigmentation gene ASIP and four candidate genes that may contribute to feather nanostructure development. Contrary to the prediction of convergent evolution of island melanism, we detected signatures of a selective sweep in genomic regions containing ASIP and SCUBE2 not in the black subspecies but in the blue subspecies, which possesses many derived SNPs in these regions, suggesting that the mainland subspecies has re-evolved a blue plumage from a black ancestor. This proposed re-evolution was likely driven by a preexisting female preference. Our findings provide new insight into the evolution of plumage coloration in island versus continental populations, and, importantly, we identify candidate genes that likely play roles in the development and evolution of feather structural coloration.
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Melanosis , Passeriformes , Pájaros Cantores , Animales , Pájaros Cantores/genética , Australia , Passeriformes/genética , Polimorfismo de Nucleótido Simple , Plumas , Pigmentación , ColorRESUMEN
BACKGROUND: Regulation of transcription by DNA methylation in 5'-CpG-3' context is a widespread mechanism allowing differential expression of genetically identical cells to persist throughout development. Consequently, differences in DNA methylation can reinforce variation in gene expression among cells, tissues, populations, and species. Despite a surge in studies on DNA methylation, we know little about the importance of DNA methylation in population differentiation and speciation. Here we investigate the regulatory and evolutionary impact of DNA methylation in five tissues of two Ficedula flycatcher species and their naturally occurring F1 hybrids. RESULTS: We show that the density of CpG in the promoters of genes determines the strength of the association between DNA methylation and gene expression. The impact of DNA methylation on gene expression varies among tissues with the brain showing unique patterns. Differentially expressed genes between parental species are predicted by genetic and methylation differentiation in CpG-rich promoters. However, both these factors fail to predict hybrid misexpression suggesting that promoter mismethylation is not a main determinant of hybrid misexpression in Ficedula flycatchers. Using allele-specific methylation estimates in hybrids, we also determine the genome-wide contribution of cis- and trans effects in DNA methylation differentiation. These distinct mechanisms are roughly balanced in all tissues except the brain, where trans differences predominate. CONCLUSIONS: Overall, this study provides insight on the regulatory and evolutionary impact of DNA methylation in songbirds.
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Islas de CpG , Metilación de ADN , Regiones Promotoras Genéticas , Pájaros Cantores , Animales , Pájaros Cantores/genética , Islas de CpG/genética , Hibridación Genética , Evolución Molecular , Evolución Biológica , Regulación de la Expresión GénicaRESUMEN
BACKGROUND: Resolving the phylogeny of rapidly radiating lineages presents a challenge when building the Tree of Life. An Old World avian family Prunellidae (Accentors) comprises twelve species that rapidly diversified at the Pliocene-Pleistocene boundary. RESULTS: Here we investigate the phylogenetic relationships of all species of Prunellidae using a chromosome-level de novo assembly of Prunella strophiata and 36 high-coverage resequenced genomes. We use homologous alignments of thousands of exonic and intronic loci to build the coalescent and concatenated phylogenies and recover four different species trees. Topology tests show a large degree of gene tree-species tree discordance but only 40-54% of intronic gene trees and 36-75% of exonic genic trees can be explained by incomplete lineage sorting and gene tree estimation errors. Estimated branch lengths for three successive internal branches in the inferred species trees suggest the existence of an empirical anomaly zone. The most common topology recovered for species in this anomaly zone was not similar to any coalescent or concatenated inference phylogenies, suggesting presence of anomalous gene trees. However, this interpretation is complicated by the presence of gene flow because extensive introgression was detected among these species. When exploring tree topology distributions, introgression, and regional variation in recombination rate, we find that many autosomal regions contain signatures of introgression and thus may mislead phylogenetic inference. Conversely, the phylogenetic signal is concentrated to regions with low-recombination rate, such as the Z chromosome, which are also more resistant to interspecific introgression. CONCLUSIONS: Collectively, our results suggest that phylogenomic inference should consider the underlying genomic architecture to maximize the consistency of phylogenomic signal.
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Flujo Génico , Genómica , Pájaros Cantores , Filogenia , Genómica/métodos , GenomaRESUMEN
Migratory divides, hybrid zones between populations that use different seasonal migration routes, are hypothesised to contribute to speciation. Specifically, relative to parental species, hybrids at divides are predicted to exhibit (1) intermediate migratory behaviour and (2) reduced fitness as a result. We provide the first direct test of the second prediction here with one of the largest existing avian tracking datasets, leveraging a divide between Swainson's thrushes where the first prediction is supported. Using detection rates as a proxy for survival, our results supported the migratory divide hypothesis with lower survival rates for hybrids than parental forms. This finding was juvenile-specific (vs. adults), suggesting selection against hybrids is stronger earlier in life. Reduced hybrid survival was not explained by selection against intermediate phenotypes or negative interactions among phenotypes. Additional work connecting specific features of migration is needed, but these patterns provide strong support for migration as an ecological driver of speciation.
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Pájaros Cantores , Animales , Pájaros Cantores/genética , Migración Animal , Fenotipo , Estaciones del AñoRESUMEN
Insects are key components of food chains, and monitoring data provides new opportunities to identify trophic relationships at broad spatial and temporal scales. Here, combining two monitoring datasets from Great Britain, we reveal how the population dynamics of the blue tit Cyanistes caeruleus are influenced by the abundance of moths - a core component of their breeding diet. We find that years with increased population growth for blue tits correlate strongly with high moth abundance, but population growth in moths and birds is less well correlated; suggesting moth abundance directly affects bird population change. Next, we identify moths that are important components of blue tit diet, recovering associations to species previously identified as key food sources such as the winter moth Operoptera brumata. Our work provides new evidence that insect abundance impacts bird population dynamics in natural communities and provides insight into spatial diet turnover at a national-scale.
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Mariposas Nocturnas , Pájaros Cantores , Animales , Insectos , Cadena Alimentaria , Estaciones del AñoRESUMEN
AbstractMany animals exhibit contrast between their dorsal coloration and their ventral coloration. If selection acts differently on dorsal versus ventral coloration, ancestral covariance between these traits should break down, eventually leading to independent modules of trait evolution. Here, we compare the evolution of feather color across body regions for a clade of Australasian songbirds (Meliphagoidea). We find evidence for three modules of covarying color regions. Among these modules, ventral feathers evolve with high lability, evolving at three times the rate of dorsal plumage and 20 times the rate of flight feathers. While both dorsal plumage and ventral plumage are darker in areas with more precipitation and vegetation, we find that dorsal plumage is twice as similar to colors in satellite photos of background substrates. Overall, differential selection on ventral and dorsal colors likely maintains these as distinct modules over evolutionary timescales-a novel explanation for dorsoventral contrast in pigmentation.
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Passeriformes , Pájaros Cantores , Animales , Pájaros Cantores/genética , Fenotipo , Pigmentación/genética , Plumas , ColorRESUMEN
AbstractVocal production learning (the capacity to learn to produce vocalizations) is a multidimensional trait that involves different learning mechanisms during different temporal and socioecological contexts. Key outstanding questions are whether vocal production learning begins during the embryonic stage and whether mothers play an active role in this through pupil-directed vocalization behaviors. We examined variation in vocal copy similarity (an indicator of learning) in eight species from the songbird family Maluridae, using comparative and experimental approaches. We found that (1) incubating females from all species vocalized inside the nest and produced call types including a signature "B element" that was structurally similar to their nestlings' begging call; (2) in a prenatal playback experiment using superb fairy wrens (Malurus cyaneus), embryos showed a stronger heart rate response to playbacks of the B element than to another call element (A); and (3) mothers that produced slower calls had offspring with greater similarity between their begging call and the mother's B element vocalization. We conclude that malurid mothers display behaviors concordant with pupil-directed vocalizations and may actively influence their offspring's early life through sound learning shaped by maternal call tempo.
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Passeriformes , Pájaros Cantores , Animales , Femenino , Humanos , Madres , Vocalización Animal/fisiología , Pájaros Cantores/fisiología , AprendizajeRESUMEN
AbstractDespite avid interest in life history trade-offs and the costs of reproduction, evidence that increased parental allocation reduces subsequent breeding productivity is mixed. This uncertainty may be attributable to environmental heterogeneity in space and time, necessitating experiments across a range of ecological contexts. Over three breeding seasons, we cross-fostered clutches between nests to manipulate incubation duration in a wild population of Carolina wrens, a species in which only females incubate, to test for a cost of incubation on current and future reproduction. Prolonged incubation affected maternal productivity in a manner dependent on the current environment and initial investment in eggs, suggesting that incubation is optimized according to other components of reproduction and individual quality. Effects of incubation duration on foster nestling condition varied between years, being costly in one, beneficial in another, and neutral in the third. The proportion of young fledged, females' probability of breeding again within seasons, and subsequent clutch sizes all declined with increasing incubation effort-effects that became more pronounced as seasons progressed. Therefore, costs of incubation were almost entirely dependent on maternal quality and environmental variation, illustrating the importance of conducting experiments across a range of environmental settings for understanding the costs of reproduction and evolution of life histories.
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Pájaros Cantores , Animales , Femenino , Reproducción , Probabilidad , Estaciones del Año , IncertidumbreRESUMEN
AbstractSampling, investing time or energy to learn about the environment, allows organisms to track changes in resource distribution and quality. The use of sampling is predicted to change as a function of energy expenditure, food availability, and starvation risk, all of which can vary both within and among individuals. We studied sampling behavior in a field study with black-capped chickadees (Poecile atricapillus) and show that individuals adjust their use of sampling as a function of ambient temperature (a proxy for energy expenditure), the presence of an alternative food source (yes or no, a proxy for risk of energy shortfall), and their interaction, as predicted by models of optimal sampling. We also observed repeatable differences in sampling. Some individuals consistently sampled more, and individuals that sampled more overall also had a higher annual survival. These results are consistent with among-individual differences in resource acquisition (e.g., food caches or dominance-related differences in priority access to feeders), shaping among-individual differences in both sampling and survival, with greater resource acquisition leading to both higher sampling and higher survival. Although this explanation requires explicit testing, it is in line with several recent studies suggesting that variation in resource acquisition is a key mechanism underlying animal personality.
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Pájaros Cantores , Humanos , Animales , AprendizajeRESUMEN
AbstractIn species with resource-defense mating systems (such as most temperate-breeding songbirds), male dispersal is often considered to be limited in both frequency and spatial extent. When dispersal occurs within a breeding season, the favored explanation is ecological resource tracking. In contrast, movements of male birds associated with temporary emigration, such as polyterritoriality (i.e., defense of an additional location after attracting a female in the initial territory), are usually attributed to mate searching. We suggest that male dispersal and polyterritoriality are functionally related and that mate searching may be a unifying hypothesis for predicting the within-season movements of male songbirds. Here, we test three key predictions derived from this hypothesis in Wood Warblers (Phylloscopus sibilatrix). We collected data on the spatial behavior of 107 males between 2017 and 2019 and related male movements to a new territory (in both a dispersal and a polyterritorial context) to mating potential in the current territory. Most males dispersed from their territories within days or weeks after failing to attract a female, despite occupying territories in apparently suitable habitat. Probability of polyterritoriality by paired males increased after the peak fertile period of their mate. Males never dispersed following nest predation if the female remained to renest. Thus, our data are consistent with the hypothesis that both movement types are functionally related to mate searching.
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Pájaros Cantores , Animales , Femenino , Masculino , Conducta Sexual Animal , Estaciones del Año , Ecosistema , ReproducciónRESUMEN
Cooperation may emerge from intrinsic factors such as social structure and extrinsic factors such as environmental conditions. Although these factors might reinforce or counteract each other, their interaction remains unexplored in animal populations. Studies on multilevel societies suggest a link between social structure, environmental conditions and individual investment in cooperative behaviours. These societies exhibit flexible social configurations, with stable groups that overlap and associate hierarchically. Structure can be seasonal, with upper-level units appearing only during specific seasons, and lower-level units persisting year-round. This offers an opportunity to investigate how cooperation relates to social structure and environmental conditions. Here, we study the seasonal multilevel society of superb fairy-wrens (Malurus cyaneus), observing individual responses to experimental playback of conspecific distress calls. Individuals engaged more in helping behaviour and less in aggressive/territorial song during the harsher non-breeding season compared to the breeding season. The increase in cooperation was greater for breeding group members than for members of the same community, the upper social unit, comprised of distinct breeding groups in association. Results suggest that the interaction between social structure and environmental conditions drives the seasonal switch in cooperation, supporting the hypothesis that multilevel societies can emerge to increase cooperation during harsh environmental conditions.
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Passeriformes , Pájaros Cantores , Humanos , Animales , Pájaros Cantores/fisiología , Conducta Cooperativa , Territorialidad , Conducta de AyudaRESUMEN
Recombination is a central evolutionary process that reshuffles combinations of alleles along chromosomes, and consequently is expected to influence the efficacy of direct selection via Hill-Robertson interference. Additionally, the indirect effects of selection on neutral genetic diversity are expected to show a negative relationship with recombination rate, as background selection and genetic hitchhiking are stronger when recombination rate is low. However, owing to the limited availability of recombination rate estimates across divergent species, the impact of evolutionary changes in recombination rate on genomic signatures of selection remains largely unexplored. To address this question, we estimate recombination rate in two Ficedula flycatcher species, the taiga flycatcher (Ficedula albicilla) and collared flycatcher (Ficedula albicollis). We show that recombination rate is strongly correlated with signatures of indirect selection, and that evolutionary changes in recombination rate between species have observable impacts on this relationship. Conversely, signatures of direct selection on coding sequences show little to no relationship with recombination rate, even when restricted to genes where recombination rate is conserved between species. Thus, using measures of indirect and direct selection that bridge micro- and macro-evolutionary timescales, we demonstrate that the role of recombination rate and its dynamics varies for different signatures of selection.
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Passeriformes , Pájaros Cantores , Animales , Pájaros Cantores/genética , Selección Genética , Genoma , Passeriformes/genética , Recombinación GenéticaRESUMEN
Birdsongs are among the most distinctive animal signals. Their evolution is thought to be shaped simultaneously by habitat structure and by the constraints of morphology. Habitat structure affects song transmission and detectability, thus influencing song (the acoustic adaptation hypothesis), while body size and beak size and shape necessarily constrain song characteristics (the morphological constraint hypothesis). Yet, support for the acoustic adaptation and morphological constraint hypotheses remains equivocal, and their simultaneous examination is infrequent. Using a phenotypically diverse Australasian bird clade, the honeyeaters (Aves: Meliphagidae), we compile a dataset consisting of song, environmental, and morphological variables for 163 species and jointly examine predictions of these two hypotheses. Overall, we find that body size constrains song frequency and pace in honeyeaters. Although habitat type and environmental temperature influence aspects of song, that influence is indirect, likely via effects of environmental variation on body size, with some evidence that elevation constrains the evolution of song peak frequency. Our results demonstrate that morphology has an overwhelming influence on birdsong, in support of the morphological constraint hypothesis, with the environment playing a secondary role generally via body size rather than habitat structure. These results suggest that changing body size (a consequence of both global effects such as climate change and local effects such as habitat transformation) will substantially influence the nature of birdsong.
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Tamaño Corporal , Vocalización Animal , Animales , Pájaros Cantores/fisiología , Pájaros Cantores/anatomía & histología , Ecosistema , Evolución BiológicaRESUMEN
During spring migration, nocturnal migrants attempt to minimize their travel time to reach their breeding grounds early. However, how they behave and respond to unfavourable conditions during their springtime travels is much less understood. In this study, we reveal the effects of atmospheric factors on nocturnal bird migration under adverse conditions during spring and autumn, based on one of the most detailed bird migration studies globally, using radar data from 13 deployments over a period of seven years (2014-2020) in the Levant region. Using ERA5 reanalysis data, we found that migratory birds maintain similar ground speeds in both autumn and spring migrations, but during spring, when encountering unfavourable winds, they put more effort into maintaining their travel speed by increasing self-powered airspeed by 18%. Moreover, we report for the first time that spring migrants showed less selectivity to wind conditions and migrated even under unfavourable headwind and crosswind conditions. Interestingly, we discovered that temperature was the most important weather parameter, such that warm weather substantially increased migration intensities in both seasons. Our results enhance our understanding of bird migration over the Levant region, one of the world's largest and most important migration flyways, and the factors controlling it. This information is essential for predicting bird migration, which-especially under the ongoing anthropogenic changes-is of high importance.