Recent natural selection causes adaptive evolution of an avian polygenic trait

Recent natural selection in a wild bird Many studies have found evidence of rapid evolution in response to environmental change. In most cases, there has been some suggestion of which traits might be most responsive ahead of time. Bosse et al. turn this approach on its head by using genomic regions with a signature of selection to identify traits that are changing. In great tits (Parus major) in the United Kingdom, genomic regions showing selection invariably contained genes associated with bill growth. Indeed, U.K. birds not only have longer bills, but these longer bills are associated with increased fitness. These changes likely reflect an increase in domestic garden bird feeders over the past several decades. Science, this issue p. 365 Genomic regions under selection reveal that bills have lengthened in great tits in the UK. We used extensive data from a long-term study of great tits (Parus major) in the United Kingdom and Netherlands to better understand how genetic signatures of selection translate into variation in fitness and phenotypes. We found that genomic regions under differential selection contained candidate genes for bill morphology and used genetic architecture analyses to confirm that these genes, especially the collagen gene COL4A5, explained variation in bill length. COL4A5 variation was associated with reproductive success, which, combined with spatiotemporal patterns of bill length, suggested ongoing selection for longer bills in the United Kingdom. Last, bill length and COL4A5 variation were associated with usage of feeders, suggesting that longer bills may have evolved in the United Kingdom as a response to supplementary feeding.

[1]  C. Jiggins,et al.  Towards the identification of the loci of adaptive evolution , 2015, Methods in ecology and evolution.

[2]  M. Skolnick,et al.  Identification of mutations in the COL4A5 collagen gene in Alport syndrome. , 1990, Science.

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

[4]  H. Hoekstra,et al.  Molecular spandrels: tests of adaptation at the genetic level , 2011, Nature Reviews Genetics.

[5]  Kai Zeng,et al.  Evolutionary signals of selection on cognition from the great tit genome and methylome , 2016, Nature Communications.

[6]  H. Hoekstra,et al.  Molecular spandrels: tests of adaptation at the genetic level , 2011, Nature Reviews Genetics.

[7]  C. Haley,et al.  Genomewide Rapid Association Using Mixed Model and Regression: A Fast and Simple Method For Genomewide Pedigree-Based Quantitative Trait Loci Association Analysis , 2007, Genetics.

[8]  Pardis C Sabeti,et al.  Detecting recent positive selection in the human genome from haplotype structure , 2002, Nature.

[9]  A. Hendry,et al.  Human influences on rates of phenotypic change in wild animal populations , 2008, Molecular ecology.

[10]  Cameron D. Palmer,et al.  Evidence of widespread selection on standing variation in Europe at height-associated SNPs , 2012, Nature Genetics.

[11]  Renaud Vitalis,et al.  rehh: an R package to detect footprints of selection in genome-wide SNP data from haplotype structure , 2012, Bioinform..

[12]  G. Coop,et al.  A Population Genetic Signal of Polygenic Adaptation , 2013, PLoS genetics.

[13]  T. de Ravel,et al.  Deletions in the VPS13B (COH1) gene as a cause of Cohen syndrome , 2009, Human mutation.

[14]  Andreas Fregin,et al.  Mutations in VKORC1 cause warfarin resistance and multiple coagulation factor deficiency type 2 , 2004, Nature.

[15]  B. Grant,et al.  Unpredictable Evolution in a 30-Year Study of Darwin's Finches , 2002, Science.

[16]  M. Fellowes,et al.  Wild Bird Feeding in an Urban Area: Intensity, Economics and Numbers of Individuals Supported , 2015 .

[17]  Kevin R. Thornton,et al.  A New Approach for Using Genome Scans to Detect Recent Positive Selection in the Human Genome , 2007, PLoS biology.

[18]  Pornpimol Charoentong,et al.  ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks , 2009, Bioinform..

[19]  M Erbe,et al.  Improving accuracy of genomic predictions within and between dairy cattle breeds with imputed high-density single nucleotide polymorphism panels. , 2012, Journal of dairy science.

[20]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[21]  Trevor Hastie,et al.  Regularization Paths for Generalized Linear Models via Coordinate Descent. , 2010, Journal of statistical software.

[22]  Yurii S. Aulchenko,et al.  BIOINFORMATICS APPLICATIONS NOTE doi:10.1093/bioinformatics/btm108 Genetics and population analysis GenABEL: an R library for genome-wide association analysis , 2022 .

[23]  B. Benyamin,et al.  EigenGWAS: finding loci under selection through genome-wide association studies of eigenvectors in structured populations , 2015, Heredity.

[24]  H. Zou,et al.  Regularization and variable selection via the elastic net , 2005 .

[25]  A. Gosler.  Pattern and process in the bill morphology of the Great Tit Parus major , 2008 .

[26]  Jarrod D. Hadfield,et al.  MCMC methods for multi-response generalized linear mixed models , 2010 .

[27]  P. Visscher,et al.  GCTA: a tool for genome-wide complex trait analysis. , 2011, American journal of human genetics.

[28]  W. G. Hill,et al.  Genome partitioning of genetic variation for complex traits using common SNPs , 2011, Nature Genetics.

[29]  Jarrod Had.  MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package , 2010 .

[30]  O. Delaneau,et al.  A linear complexity phasing method for thousands of genomes , 2011, Nature Methods.

[31]  N. Hagiwara.  Sox6, jack of all trades: A versatile regulatory protein in vertebrate development , 2011, Developmental dynamics : an official publication of the American Association of Anatomists.

[32]  B. Voelkl,et al.  Individual variation in winter supplementary food consumption and its consequences for reproduction in wild birds , 2016 .

[33]  M. Grabherr,et al.  Evolution of Darwin’s finches and their beaks revealed by genome sequencing , 2015, Nature.

[34]  H. Hoekstra,et al.  On the Origin and Spread of an Adaptive Allele in Deer Mice , 2009, Science.

[35]  H. Hoekstra,et al.  Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits , 2008, Heredity.

[36]  H. Kronenberg.  PTHrP and Skeletal Development , 2006, Annals of the New York Academy of Sciences.

[37]  Darryl N. Jones,et al.  Feeding birds in our towns and cities: a global research opportunity , 2008 .

[38]  P. Tryjanowski,et al.  Who started first? Bird species visiting novel birdfeeders , 2015, Scientific Reports.

[39]  P. Visscher,et al.  Simultaneous Discovery, Estimation and Prediction Analysis of Complex Traits Using a Bayesian Mixture Model , 2015, PLoS genetics.

[40]  K. Hobson,et al.  Contemporary Evolution of Reproductive Isolation and Phenotypic Divergence in Sympatry along a Migratory Divide , 2009, Current Biology.

[41]  B. Grant,et al.  A beak size locus in Darwin’s finches facilitated character displacement during a drought , 2016, Science.

[42]  Joseph K. Pickrell,et al.  The Genetics of Human Adaptation: Hard Sweeps, Soft Sweeps, and Polygenic Adaptation , 2010, Current Biology.

[43]  Ericka Stricklin-Parker,et al.  Ann , 2005 .

[44]  B. Sheldon,et al.  Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle , 2009, Proceedings of the Royal Society B: Biological Sciences.

[45]  J. Slate,et al.  The design and cross‐population application of a genome‐wide SNP chip for the great tit Parus major , 2012, Molecular ecology resources.

[46]  A Ballabio,et al.  Alport syndrome, mental retardation, midface hypoplasia, and elliptocytosis: a new X linked contiguous gene deletion syndrome? , 1998, Journal of medical genetics.