1 Introduction

Understanding genetic adaptation in avian species is crucial for several reasons. Birds are among the most diverse and widely distributed vertebrates, occupying a variety of ecological niches across the globe. This diversity makes them excellent models for studying evolutionary processes and genetic adaptation. Genetic adaptation allows avian species to survive and thrive in changing environments, which is essential for their conservation and management. Moreover, birds often serve as indicators of environmental health, making their study relevant for broader ecological and environmental monitoring (Teplitsky et al., 2014; Duc and Schöneberg, 2016; Josephs, 2020).

Rapid environmental changes refer to significant alterations in climate, habitat, and ecosystems that occur over short time scales, often due to anthropogenic activities. These changes include global warming, habitat fragmentation, pollution, and the introduction of invasive species. Such rapid changes can impose severe selective pressures on wildlife, necessitating quick adaptive responses for survival (Charmantier et al., 2008; Lai et al., 2019).

Genetic adaptation is particularly relevant in the context of climate change, habitat loss, and human activities. Climate change can alter the availability of resources, timing of breeding seasons, and migration patterns, requiring birds to adapt quickly to new conditions. Habitat loss and fragmentation, often driven by urbanization and deforestation, can isolate populations and reduce genetic diversity, making adaptation more challenging (Kozakiewicz et al., 2018). Human activities, such as pollution and the introduction of invasive species, can also create new selective pressures that necessitate rapid genetic changes for survival (Andrew et al., 2018).

This study is to synthesize current knowledge on genetic adaptation in avian species in response to rapid environmental changes. It will identify key genetic mechanisms that facilitate adaptation in birds, evaluate the role of standing genetic variation and new mutations in adaptive processes, assess the impact of phenotypic plasticity and gene expression changes on adaptation, and highlight the constraints and limitations of genetic adaptation in the face of rapid environmental changes. By achieving these objectives, This study expects to provide a comprehensive understanding of how avian species adapt genetically to rapidly changing environments, which will be crucial for predicting future adaptive responses and informing conservation strategies to mitigate the impacts of environmental changes on bird populations.

2 Mechanisms of Genetic Adaptation in Avian Species

2.1 Natural selection and its role in avian genetic adaptation

Natural selection is a fundamental mechanism driving genetic adaptation in avian species. It operates by favoring individuals with advantageous traits that enhance survival and reproductive success in specific environments. For instance, studies on house finches (Haemorhous mexicanus) have shown that natural selection can lead to adaptive evolution by influencing genes related to fat metabolism, neurodevelopment, and ion binding, which are crucial for coping with environmental stresses (Backström et al., 2013). Additionally, research on songbirds has demonstrated that preexisting genetic variations play a predominant role in local adaptation, suggesting that natural selection acts on these standing genetic variants to facilitate rapid adaptation to new environmental conditions (Lai et al., 2019).

2.2 Genetic mutations and their impact on avian populations

Genetic mutations introduce new genetic variations into populations, which can be acted upon by natural selection. These mutations can lead to significant evolutionary changes if they confer a survival advantage. For example, the spleen transcriptome analysis of house finches revealed a higher ratio of nonsynonymous to synonymous substitutions, indicating that genetic mutations contribute to adaptive evolution in passerine birds (Backström et al., 2013). Moreover, the study on nocturnal adaptation in birds highlights how genetic changes support adaptation to dim-light environments, showcasing the role of mutations in facilitating ecological niche shifts (Duc and Schöneberg, 2016).

2.3 Gene flow and genetic drift in avian species

Gene flow and genetic drift are additional mechanisms influencing genetic adaptation in avian species. Gene flow, the transfer of genetic material between populations, can introduce new genetic variations that enhance adaptability. Conversely, genetic drift, the random fluctuation of allele frequencies, can lead to significant genetic changes, especially in small populations. Research on long-term avian studies has shown that genetic correlations can constrain the rate of adaptation, indicating that gene flow and genetic drift play complex roles in shaping evolutionary trajectories (Teplitsky et al., 2014). Furthermore, the study on the adaptation of songbirds to different altitudes underscores the importance of gene flow in maintaining genetic diversity and facilitating local adaptation (Yang et al., 2019).

2.4 Role of epigenetics in avian adaptation to environmental changes

Epigenetic mechanisms, such as DNA methylation, histone modifications, and non-coding RNAs, play a crucial role in avian adaptation to environmental changes. These mechanisms can induce phenotypic changes without altering the underlying DNA sequence, allowing for rapid and reversible adaptation. For instance, a study on the epigenetic variation between two populations of Darwin’s finches, Geospiza fortis and G. fuliginosa (Figure 1), suggesting that DNA methylation contributes to local adaptation (Platt et al., 2015; McNew et al., 2017). Additionally, studies on invasive species have highlighted the importance of epigenetic variation in enabling rapid adaptation to new environments, with DNA methylation patterns being strongly influenced by local environmental conditions (Carneiro and Lyko, 2020; Chen et al., 2022). The concept of “bet hedging” against climate change further illustrates how epigenetic mechanisms can create multiple phenotypes from the same genotype, enhancing survival during extreme weather events (Burggren and Mendez-Sanchez, 2023).

Figure 1 Study sites and species (Adopted from McNew et al., 2017) Image caption: (A) The Galápagos Archipelago. (B) Santa Cruz Island; Roads are indicated by narrow grey lines and study sites by red Xs. (C) Geospiza fortis; photo by J.A.H.K. (D) Geospiza fuliginosa; photo by S.A.K. Maps in (A) and (B) are modified from © 2016 Google (Adopted from McNew et al., 2017)

3 Environmental Stressors Affecting Avian Species

3.1 Climate change: temperature fluctuations and altered precipitation patterns

Climate change is a significant environmental stressor that affects avian species through temperature fluctuations and altered precipitation patterns. These changes can influence various aspects of avian life, including growth, development, and survival. For instance, weather conditions such as air temperature, rainfall, wind speed, and solar radiation have been shown to impact nestling growth and development, which can have long-lasting effects on adult phenotypes and fitness (Sauve et al., 2021). Additionally, climate warming has been correlated with body size reductions in North American migratory birds, although species with larger relative brain sizes exhibit weaker phenotypic responses, suggesting that cognitive abilities may buffer some species from the impacts of warming temperatures (Baldwin et al., 2022).

3.2 Habitat destruction and fragmentation

Habitat destruction and fragmentation pose severe threats to avian species by reducing available habitats and isolating populations. This can lead to inbreeding, loss of genetic variation, and increased extinction rates, particularly under stressful conditions (Frankham, 2005). Fragmented populations may also experience reduced adaptive evolutionary potential, making it challenging for them to cope with environmental changes. The persistence of avian species in fragmented habitats often depends on their ability to adapt to local conditions, which can be facilitated by standing genetic variation (Yang et al., 2019).

3.3 Pollution and its genetic implications

Pollution, particularly from industrial sources, can act as a selective pressure on avian populations, leading to genetic adaptations. Such rapid evolutionary rescue is less likely in species with smaller population sizes due to the complexity of adaptive phenotypes and potential fitness costs. The genetic architecture underlying these adaptations often involves multiple regions under selection, reflecting complex responses to diverse stressors.

3.4 Introduction of invasive species and competition

The introduction of invasive species can lead to increased competition for resources, which can drive local adaptation in native avian species. The house sparrow (Passer domesticus), introduced to Australia from Europe, has been used as a model to study local adaptation in invasive species. Genomic analyses have identified loci subject to selection across varied climates, with some outlier genes linked to traits important for local adaptation, such as heat-shock proteins and immune response genes (Andrew et al., 2018). This highlights the role of genetic adaptation in enabling invasive species to thrive in new environments.

3.5 Anthropogenic factors: urbanization, agriculture, and industry

Urbanization, agriculture, and industrial activities are major anthropogenic factors that impact avian species. These activities can lead to habitat modification, pollution, and increased human-wildlife interactions, all of which can exert selective pressures on avian populations. For instance, urbanization can alter selection pressures on growth traits, necessitating adaptive plastic or evolutionary changes in response to changing environments (Sauve et al., 2021). Additionally, the evolutionary potential of avian populations is closely linked to their preexisting genetic diversity, which can influence their ability to adapt to anthropogenic changes.

4 Case Study: Genetic Adaptation in Arctic Terns

4.1 Overview of the environmental challenges faced by arctic terns

Arctic terns (Sterna paradisaea) are renowned for their extraordinary migratory behavior, undertaking the longest known annual migration of any organism, traveling between breeding sites in the Arctic and temperate regions to survival and molting areas in the Antarctic pack-ice zone (Alerstam et al., 2019). This extensive migration exposes them to a wide range of environmental conditions, including varying temperatures, food availability, and predation pressures. During the breeding season, Arctic terns are central place foragers, restricted to the first 50 cm of the water column, and must adjust their foraging behaviors to compensate for extrinsic factors such as local weather and fisheries (Morten et al., 2022). Additionally, contamination of Arctic marine environments with persistent organic pollutants (POPs) poses a significant challenge, although studies have shown that male Arctic terns can rapidly eliminate these contaminants during the breeding season (Mallory et al., 2019).

4.2 Detailed analysis of genetic changes observed in this species

Recent genomic studies have provided insights into the genetic adaptations of Arctic terns to their challenging environments. For instance, the use of light-level geolocators has revealed significant segregation in time and space between tern populations in the same flyway, suggesting adaptive genetic differentiation based on migration patterns and environmental conditions encountered during their extensive journeys (Alerstam et al., 2019). Furthermore, the genetic basis of phenotypic plasticity in Arctic terns has been explored through the study of ecomorphs in related species, which show substantial changes in genotype-phenotype relationships in response to different environmental conditions (Küttner et al., 2014). These findings suggest that Arctic terns may also possess hidden genetic variation that evolves with ecological specialization, allowing them to adapt to diverse and changing environments.

4.3 Discussion on the adaptive significance of these genetic changes

The genetic adaptations observed in Arctic terns are crucial for their survival and reproductive success in the face of rapid environmental changes. The ability to rapidly eliminate contaminants, as seen in male Arctic terns, likely provides a significant advantage in maintaining health and reproductive fitness during the breeding season (Mallory et al., 2019). The observed genetic differentiation based on migration patterns and environmental conditions highlights the importance of local adaptation in ensuring that Arctic terns can exploit optimal foraging areas and avoid competition and predation (Figure 2) (Alerstam et al., 2019). Additionally, the potential for hidden genetic variation to be exposed under different environmental conditions suggests that Arctic terns have a robust capacity for phenotypic plasticity, enabling them to respond to and thrive in a wide range of ecological niches.

Figure 2 Map (Mercator projection) showing estimated locations of arctic terns from the Baltic Sea during their annual migration cycle (Adopted from Alerstam et al., 2019) Image caption: Daily locations based on geolocator data for 12 annual journeys by eight individuals are shown for all journeys combined to illustrate the overall global migration pattern for the study population. Locations are missing due to uncertain and invalid latitude data during periods around the autumn and spring equinoxes. Arrows indicate the most likely movement patterns based on longitude data during the equinox periods, eastward into the Indian Ocean around the autumn equinox and toward northeast (first) and northwest (later) from the Weddell Sea up the southern Atlantic Ocean around the spring equinox. Small arrows indicate southeastward crossing of the Antarctic Convergence in the longitudinal sector from 80E and eastward. Locations have been provisionally plotted during the terns’ wintering period in the Antarctic in spite of the fact that latitude could not be properly estimated but only inferred to be south of 60S during the southern polar summer. The Mercator projection is conformal and true to compass direction. However, it is not true to distance and area, with polar regions greatly exaggerated in size (Adopted from Alerstam et al., 2019)

5 Phenotypic Plasticity vs. Genetic Adaptation

5.1 Definition and examples of phenotypic plasticity in avian species

Phenotypic plasticity refers to the ability of a single genotype to produce different phenotypes in response to varying environmental conditions. This adaptive mechanism allows organisms to cope with environmental changes without genetic alterations. In avian species, phenotypic plasticity can manifest in various ways. For instance, zebra finch mothers exposed to heat stress can induce changes in their offspring, such as altered heart rates and increased eggshell pore density, which are positively correlated with survival under high temperatures (Hoffman et al., 2021). Another example is the great tit (Parus major), which adjusts its reproductive timing in response to environmental changes, allowing the population to closely track rapid climate changes.

5.2 Comparison between phenotypic plasticity and genetic adaptation

Phenotypic plasticity and genetic adaptation are two distinct mechanisms through which organisms can respond to environmental changes. Phenotypic plasticity involves immediate, reversible changes in phenotype without altering the underlying genetic code. In contrast, genetic adaptation involves changes in allele frequencies within a population over generations, leading to permanent alterations in phenotype.

Phenotypic plasticity acts as a rapid-response mechanism, enabling individuals to survive sudden environmental changes. For example, plastic responses in avian species can include behavioral adjustments to human disturbances, such as reduced flushing distances and changes in social behavior (Jiménez et al., 2013). On the other hand, genetic adaptation is a slower process that involves the selection of advantageous traits over multiple generations. Studies have shown that genetic changes often reverse plastic phenotypic changes to recover fitness after environmental shifts, indicating that plasticity serves as an emergency response rather than a stepping stone to genetic adaptation (Ho and Zhang, 2018).

5.3 Contribution of both mechanisms to avian survival in changing environments

Both phenotypic plasticity and genetic adaptation play crucial roles in avian survival amidst rapid environmental changes. Phenotypic plasticity allows birds to quickly adjust to new conditions, providing an immediate buffer against environmental stressors. For instance, urban birds exhibit higher phenotypic variation in breeding phenology compared to their non-urban counterparts, which may result from plastic responses to the heterogeneous urban environment (Capilla-Lasheras et al., 2021). This plasticity can be vital for short-term survival and maintaining population viability.

Genetic adaptation, while slower, ensures long-term survival by gradually optimizing phenotypes to the new environmental conditions. For example, in the Karoo scrub-robin, genetic variation underlying energy metabolic pathways and gut microbiome composition facilitates adaptation to arid conditions, highlighting the role of genetic adaptation in coping with extreme environments (Ribeiro et al., 2019).

6 Impact of Climate Change on Avian Genetic Adaptation

6.1 Detailed discussion on how climate change specifically drives genetic adaptation

Climate change exerts significant pressure on avian species, driving genetic adaptation through various mechanisms. One primary way is by altering environmental conditions such as temperature, precipitation, and wind patterns, which in turn affect the availability of resources and habitat suitability. These changes can lead to shifts in phenotypic traits that are subject to natural selection. For instance, variations in weather conditions have been shown to impact nestling growth and development, which are critical for survival and reproductive success. Understanding how these environmental factors influence growth trajectories can help predict population changes and adaptive responses (Sauve et al., 2021).

Moreover, climate change can impose evolutionary constraints by altering the selection pressures on morphological and phenological traits. For example, a meta-analysis revealed that while global warming has not systematically affected morphological traits in birds, it has advanced phenological traits such as breeding times. These phenological shifts are adaptive for some species but are often incomplete, indicating an evolutionary load that may threaten species persistence. Additionally, genetic correlations among traits can constrain the rate of adaptation, as seen in studies where multivariate constraints reduced the predicted rate of adaptation by 28% (Teplitsky et al., 2014).

6.2 Examples of avian species that have shown genetic adaptation to climate change

Several avian species have demonstrated genetic adaptation to climate change. The great tit (Parus major) in the United Kingdom is a notable example. Over a 47-year study, this species exhibited phenotypic plasticity, allowing it to closely track environmental changes. This plasticity enabled the population to adjust behaviorally to the changing climate, although the response appeared to be fixed within the population.

Another example is the collared flycatcher (Ficedula albicollis), where studies have shown that early environmental effects, rather than genetic heritability, significantly influence resting metabolic rate (RMR). This suggests that parental effects and early-life conditions play a crucial role in shaping adaptive responses to climate change (McFarlane et al., 2021).

Additionally, North American migratory birds have shown a decline in body size over several decades, a phenotypic response correlated with increasing temperatures. This trend indicates that natural selection is favoring smaller body sizes, which may be an adaptive response to warmer climates (Buskirk et al., 2010).

6.3 Predictions for future adaptive responses based on current genetic trends

Based on current genetic trends, future adaptive responses in avian species are likely to be complex and multifaceted. Predictions suggest that while some species may continue to exhibit phenotypic plasticity, others may face significant evolutionary constraints. For instance, the potential for evolutionary rescue through the spread of climate-adaptive genetic variation depends on a population's adaptive capacity and landscape connectivity. Enhancing landscape connectivity could facilitate the spread of adaptive traits and reduce the risk of extinction (Razgour et al., 2019).

Furthermore, the role of cognitive abilities in buffering against climate change is becoming increasingly evident. Species with larger relative brain sizes have shown weaker phenotypic responses to climate warming, suggesting that behavioral flexibility may mitigate some of the adverse effects of climate change.

7 Role of Migration in Genetic Adaptation

7.1 The influence of migratory patterns on genetic diversity

Migratory patterns play a crucial role in shaping the genetic diversity of avian species. Migration can lead to gene flow between geographically separated populations, thereby increasing genetic diversity. For instance, the willow warbler (Phylloscopus trochilus) exhibits significant genetic differences between its northern and southern subspecies, which are attributed to their distinct migratory routes and wintering areas. These differences are maintained by chromosomal inversions that are associated with migratory phenotypes and environmental gradients (Lundberg et al., 2021). Additionally, the genetic basis of migratory behavior has been demonstrated in various bird species, indicating that migratory activity and directional preferences are inherited traits. This genetic control over migration can lead to rapid evolutionary changes, as seen in obligate partial migrants where novel migratory habits can evolve in less than 25 years.

7.2 How migration affects the genetic adaptation of avian species

Migration affects genetic adaptation by enabling birds to exploit different environments, which can lead to the selection of advantageous traits. For example, the genetic determination of migration strategies in large soaring birds, such as the greater spotted eagle (Clanga clanga) and the lesser spotted eagle (Clanga pomarina), shows that genetic factors significantly influence migration timing and wintering distributions. This genetic influence allows these species to adapt their migration strategies to changing environmental conditions (Väli et al., 2018). Furthermore, the genetic correlation between migratory activity and the frequency of migrants in a population suggests that selection can act on both the incidence and the extent of migratory behavior, facilitating rapid evolutionary changes.

7.3 Case studies of migratory birds exhibiting genetic adaptation

Several case studies highlight the genetic adaptation of migratory birds:

The willow warbler’s northern and southern subspecies exhibit different migratory routes and wintering areas, maintained by chromosomal inversions. These genetic differences are associated with adaptations to distinct environmental gradients, demonstrating how migration can drive genetic divergence (Lundberg et al., 2021).

In a hybrid zone between two groups of Swainson’s thrushes, genetic mapping revealed that migratory orientation is strongly associated with specific genomic regions. This genetic basis for migration orientation suggests that these birds can rapidly adapt to new migratory routes and environmental conditions (Delmore et al., 2016).

Older, more experienced whooping cranes have been observed to innovate new migration behaviors in response to global changes. These new behaviors, such as establishing overwintering sites closer to breeding grounds, are facilitated by the age structure of the population, highlighting the role of experience and genetic adaptation in response to environmental changes (Teitelbaum et al., 2016).

These case studies illustrate the complex interplay between migration, genetic diversity, and adaptation in avian species, emphasizing the importance of genetic factors in shaping migratory behaviors and enabling rapid responses to environmental changes.

8 Conservation Implications of Avian Genetic Adaptation

8.1 How understanding genetic adaptation can inform conservation strategies

Understanding genetic adaptation in avian species is crucial for developing effective conservation strategies. Genetic adaptation refers to the changes in the genetic makeup of populations that enhance their survival and reproduction in changing environments. By studying these adaptations, conservationists can identify the genetic traits that are beneficial for survival under specific environmental conditions. For instance, research has shown that genetic correlations can significantly constrain the rate of adaptation in avian species, which could impact their ability to persist in rapidly changing environments (Teplitsky et al., 2014). Additionally, the identification of candidate genes responsible for adaptation to new ecological niches, such as nocturnality, can provide insights into the mechanisms of adaptation and inform targeted conservation efforts (Charmantier et al., 2016).

8.2 The role of genetic diversity in avian species’ long-term survival

Genetic diversity is a key factor in the long-term survival of avian species. High levels of genetic diversity increase the likelihood that some individuals within a population possess genetic variants that confer resistance to environmental changes, diseases, or other threats. Studies have shown that populations with higher genetic diversity are better equipped to adapt to new environments and changing conditions (Yin et al., 2021). For example, the genomic diversity in birds has been linked to habitat availability and life-history traits, which are critical for their conservation (Brüniche‐Olsen et al., 2021). Moreover, standing genetic variation has been identified as a predominant source for adaptation, highlighting the importance of maintaining genetic diversity within populations (Lai et al., 2019).

9 Concluding Remarks

This study has synthesized current knowledge on the genetic adaptation of avian species to rapid environmental changes, highlighting several key findings. Natural selection, genetic mutations, gene flow, and epigenetic mechanisms play crucial roles in facilitating genetic adaptation in birds, allowing them to survive and thrive in increasingly volatile environments. Climate change, habitat destruction, pollution, and invasive species introduce significant environmental stressors that drive these adaptive processes. Moreover, the role of migration has been underscored as a critical factor in shaping genetic diversity and adaptation, with migratory behaviors influencing gene flow and leading to rapid evolutionary changes.

The implications for future research are substantial. As environmental changes accelerate, there is an urgent need to deepen our understanding of the genetic mechanisms that underpin avian adaptation. Studies should focus on identifying the specific genes and genetic pathways involved in adaptation to different environmental stressors, as well as the interplay between phenotypic plasticity and genetic adaptation. Additionally, there is a need to explore the long-term effects of climate change on avian species, particularly in relation to their adaptive capacity and the potential for evolutionary rescue.

Preserving avian genetic diversity is of paramount importance in the face of rapid environmental changes. High genetic diversity within populations enhances their ability to adapt to new conditions and ensures the long-term survival of species. Conservation strategies should prioritize the protection of habitats and the maintenance of landscape connectivity to facilitate gene flow and the spread of adaptive traits. Ultimately, safeguarding avian genetic diversity is essential not only for the resilience of bird populations but also for the broader health of ecosystems in which they play a critical role.

Acknowledgments

EcoEvo Publisher appreciates the feedback from the two anonymous peer reviewers on the manuscript.

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

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