Genomic signals of selection predict climate-driven population declines in a migratory bird

Yellow warblers already in decline As the climate changes, species' ability to adapt to changing conditions may relate directly to their future persistence. Determining whether and when this will happen is challenging, however, because it is difficult to tease apart the causes of decline or maintenance. Bay et al. looked at the relationship between genomic variation and the environment in North American populations of the yellow warbler (see the Perspective by Fitzpatrick and Edelsparre). Genes linked to exploratory and migratory behavior were important for successful climate adaptation. Furthermore, populations identified as “genetically vulnerable” because of limited climate-associated genomic variation were already declining. Science, this issue p. 83; see also p. 29 Limited genetic adaptability to climate may have already led to decline in some yellow warbler populations. The ongoing loss of biodiversity caused by rapid climatic shifts requires accurate models for predicting species’ responses. Despite evidence that evolutionary adaptation could mitigate climate change impacts, evolution is rarely integrated into predictive models. Integrating population genomics and environmental data, we identified genomic variation associated with climate across the breeding range of the migratory songbird, yellow warbler (Setophaga petechia). Populations requiring the greatest shifts in allele frequencies to keep pace with future climate change have experienced the largest population declines, suggesting that failure to adapt may have already negatively affected populations. Broadly, our study suggests that the integration of genomic adaptation can increase the accuracy of future species distribution models and ultimately guide more effective mitigation efforts.

[1]  P. Leberg,et al.  Breeding Distributions of North American Bird Species Moving North as a Result of Climate Change , 2007, Conservation biology : the journal of the Society for Conservation Biology.

[2]  K. Hobson,et al.  Phylogeography and genetic structure of northern populations of the yellow warbler (Dendroica petechia) , 2000, Molecular ecology.

[3]  Peter L. Ralph,et al.  Predicting Responses to Contemporary Environmental Change Using Evolutionary Response Architectures , 2017, The American Naturalist.

[4]  C. Both,et al.  Climate change and population declines in a long-distance migratory bird , 2006, Nature.

[5]  G. Luikart,et al.  RAD Capture (Rapture): Flexible and Efficient Sequence-Based Genotyping , 2015, Genetics.

[6]  Guillaume Bouchard,et al.  Testing for Associations between Loci and Environmental Gradients Using Latent Factor Mixed Models , 2012, Molecular biology and evolution.

[7]  A. Fidler Personality-Associated Genetic Variation in Birds and Its Possible Significance for Avian Evolution, Conservation, and Welfare , 2011 .

[8]  G. Somero,et al.  The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’ , 2010, Journal of Experimental Biology.

[9]  Michael J. Fogarty,et al.  Marine Taxa Track Local Climate Velocities , 2013, Science.

[10]  Chengquan Huang,et al.  Global, 30-m resolution continuous fields of tree cover: Landsat-based rescaling of MODIS vegetation continuous fields with lidar-based estimates of error , 2013, Int. J. Digit. Earth.

[11]  Brett R. Scheffers,et al.  The broad footprint of climate change from genes to biomes to people , 2016, Science.

[12]  W. Link,et al.  The North American Breeding Bird Survey Results and Analysis , 1997 .

[13]  M. Berriman,et al.  REAPR: a universal tool for genome assembly evaluation , 2013, Genome Biology.

[14]  Ole Schulz-Trieglaff,et al.  NxTrim: optimized trimming of Illumina mate pair reads , 2014, bioRxiv.

[15]  J. Vik,et al.  Rapid Advance of Spring Arrival Dates in Long-Distance Migratory Birds , 2006, Science.

[16]  Rolf Apweiler,et al.  InterProScan - an integration platform for the signature-recognition methods in InterPro , 2001, Bioinform..

[17]  K. Hobson,et al.  Limited differentiation in microsatellite DNA variation among northern populations of the yellow warbler: evidence for male‐biased gene flow? , 2000, Molecular ecology.

[18]  Stephen R Keller,et al.  Ecological genomics meets community-level modelling of biodiversity: mapping the genomic landscape of current and future environmental adaptation. , 2015, Ecology letters.

[19]  B. Kempenaers,et al.  Haplotype structure, adaptive history and associations with exploratory behaviour of the DRD4 gene region in four great tit (Parus major) populations , 2013, Molecular ecology.

[20]  K. Hobson,et al.  Integrated Analysis of Genetic, Stable Isotope, and Banding Data Reveal Migratory Connectivity and Flyways in the Northern Yellow Warbler (Dendroica petechia; aestiva Group) , 2006 .

[21]  Angel Amores,et al.  Stacks: an analysis tool set for population genomics , 2013, Molecular ecology.

[22]  D. Schluter,et al.  Adaptation from standing genetic variation. , 2008, Trends in ecology & evolution.

[23]  Joy Bergelson,et al.  References and Notes Supporting Online Material Adaptation to Climate across the Arabidopsis Thaliana Genome , 2022 .

[24]  S. Palumbi,et al.  Multilocus Adaptation Associated with Heat Resistance in Reef-Building Corals , 2014, Current Biology.

[25]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

[26]  M. Eens,et al.  The relationship between DRD4 polymorphisms and phenotypic correlations of behaviors in the collared flycatcher , 2014, Ecology and evolution.

[27]  M. C. Urban Accelerating extinction risk from climate change , 2015, Science.

[28]  T. Juenger,et al.  Genome-environment associations in sorghum landraces predict adaptive traits , 2015, Science Advances.

[29]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[30]  S. Yeaman,et al.  Adaptation, migration or extirpation: climate change outcomes for tree populations , 2008, Evolutionary applications.

[31]  Stephen J. Smith,et al.  Gradient forests: calculating importance gradients on physical predictors. , 2012, Ecology.

[32]  Walter Pirovano,et al.  BIOINFORMATICS APPLICATIONS , 2022 .

[33]  C. Parmesan Ecological and Evolutionary Responses to Recent Climate Change , 2006 .

[34]  David H. Alexander,et al.  Fast model-based estimation of ancestry in unrelated individuals. , 2009, Genome research.

[35]  Gonçalo R. Abecasis,et al.  The variant call format and VCFtools , 2011, Bioinform..

[36]  Susanne Akesson,et al.  The genetics of migration on the move. , 2011, Trends in ecology & evolution.

[37]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[38]  J. Goudet HIERFSTAT , a package for R to compute and test hierarchical F -statistics , 2005 .

[39]  K. Shine,et al.  Intergovernmental panel on Climate change (IPCC),in encyclopedia of Enviroment and society,Vol.3 , 2007 .

[40]  Sofia M. C. Robb,et al.  MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. , 2007, Genome research.

[41]  C. Both,et al.  Effects of Spring Temperatures on the Strength of Selection on Timing of Reproduction in a Long-Distance Migratory Bird , 2015, PLoS biology.