Increased genetic diversity and immigration after West Nile virus emergence in American crows: No evidence for a genetic bottleneck

Infectious diseases can cause steep declines in wildlife populations, leading to changes in genetic diversity that may affect the susceptibility of individuals to infection and the overall resilience of populations to pathogen outbreaks. Here, we examine evidence for a genetic bottleneck in a population of American crows (Corvus brachyrhynchos) before and after the emergence of West Nile virus (WNV). More than 50% of marked birds in this population were lost over the 2‐year period of the epizootic, representing a 10‐fold increase in adult mortality. Using analyses of single‐nucleotide polymorphisms (SNPs) and microsatellite markers, we tested for evidence of a genetic bottleneck and compared levels of inbreeding and immigration in the pre‐ and post‐WNV populations. Counter to expectations, genetic diversity (allelic diversity and the number of new alleles) increased after WNV emergence. This was likely due to increases in immigration, as the estimated membership coefficients were lower in the post‐WNV population. Simultaneously, however, the frequency of inbreeding appeared to increase: Mean inbreeding coefficients were higher among SNP markers, and heterozygosity–heterozygosity correlations were stronger among microsatellite markers, in the post‐WNV population. These results indicate that loss of genetic diversity at the population level is not an inevitable consequence of a population decline, particularly in the presence of gene flow. The changes observed in post‐WNV crows could have very different implications for their response to future pathogen risks, potentially making the population as a whole more resilient to a changing pathogen community, while increasing the frequency of inbred individuals with elevated susceptibility to disease.

[1]  A. Gibson.  Genetic diversity and disease: The past, present, and future of an old idea , 2021, Evolution; international journal of organic evolution.

[2]  William Hemstrom,et al.  snpR: User friendly population genomics for SNP data sets with categorical metadata , 2021, Molecular ecology resources.

[3]  Joanna L. Kelley,et al.  Disease swamps molecular signatures of genetic‐environmental associations to abiotic factors in Tasmanian devil (Sarcophilus harrisii) populations , 2020, Evolution; international journal of organic evolution.

[4]  Joanna L. Kelley,et al.  Disease swamps molecular signatures of genetic-environmental associations to abiotic factors in Tasmanian devil (Sarcophilus harrisii) populations , 2019, bioRxiv.

[5]  A. Townsend,et al.  Apparent inbreeding preference despite inbreeding depression in the American crow , 2019, Molecular ecology.

[6]  Allison M. Weis,et al.  Low heterozygosity is associated with vector‐borne disease in crows , 2018, Ecosphere.

[7]  R. Alford,et al.  Effects of emerging infectious diseases on host population genetics: a review , 2017, Conservation Genetics.

[8]  R. Waples,et al.  Estimating contemporary effective population size in non-model species using linkage disequilibrium across thousands of loci , 2016, Heredity.

[9]  R. Wayne,et al.  Disease and freeways drive genetic change in urban bobcat populations , 2014, Evolutionary applications.

[10]  Anders Albrechtsen,et al.  ANGSD: Analysis of Next Generation Sequencing Data , 2014, BMC Bioinformatics.

[11]  G. M. Macbeth,et al.  NeEstimator v2: re‐implementation of software for the estimation of contemporary effective population size (Ne) from genetic data , 2014, Molecular ecology resources.

[12]  Menna E. Jones,et al.  Disease induced changes in gene flow patterns among Tasmanian devil populations , 2013 .

[13]  Sonya M. Hughes,et al.  The 2012 West Nile encephalitis epidemic in Dallas, Texas. , 2013, JAMA.

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

[15]  Lucie M. Gattepaille,et al.  Inferring population size changes with sequence and SNP data: lessons from human bottlenecks , 2013, Heredity.

[16]  H. Hoekstra,et al.  Double Digest RADseq: An Inexpensive Method for De Novo SNP Discovery and Genotyping in Model and Non-Model Species , 2012, PloS one.

[17]  D. Reich,et al.  Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture , 2012, Genome research.

[18]  A. Clark,et al.  Injury and paternity loss in cooperatively breeding American Crows , 2011 .

[19]  Andrew D. Miller,et al.  Condition, innate immunity and disease mortality of inbred crows , 2010, Proceedings of the Royal Society B: Biological Sciences.

[20]  J. Merilä,et al.  Rhh: an R extension for estimating multilocus heterozygosity and heterozygosity–heterozygosity correlation , 2010, Molecular ecology resources.

[21]  Miriah D. Meyer,et al.  Genome-wide synteny through highly sensitive sequence alignment: Satsuma , 2010, Bioinform..

[22]  P. L. Le Gouar,et al.  How Ebola Impacts Genetics of Western Lowland Gorilla Populations , 2009, PloS one.

[23]  A. Clark,et al.  Direct Benefits and Genetic Costs of Extrapair Paternity for Female American Crows (Corvus brachyrhynchos) , 2009, The American Naturalist.

[24]  M. Stephens,et al.  Inferring weak population structure with the assistance of sample group information , 2009, Molecular ecology resources.

[25]  R. Nichols,et al.  Population genetic patterns suggest a behavioural change in wild common frogs (Rana temporaria) following disease outbreaks (Ranavirus) , 2009, Molecular ecology.

[26]  I. Lovette,et al.  Disease-mediated inbreeding depression in a large, open population of cooperative crows , 2009, Proceedings of the Royal Society B: Biological Sciences.

[27]  I. Lovette,et al.  Reproductive partitioning and the assumptions of reproductive skew models in the cooperatively breeding American crow , 2009, Animal Behaviour.

[28]  F. Rousset.  genepop’007: a complete re‐implementation of the genepop software for Windows and Linux , 2008, Molecular ecology resources.

[29]  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.

[30]  P. Marra,et al.  West Nile virus emergence and large-scale declines of North American bird populations , 2007, Nature.

[31]  Joseph I. Hoffman,et al.  Automated binning of microsatellite alleles: problems and solutions , 2006 .

[32]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[33]  T. Kawecki,et al.  Conceptual issues in local adaptation , 2004 .

[34]  F. Balloux,et al.  Does heterozygosity estimate inbreeding in real populations? , 2004, Molecular ecology.

[35]  B. C. Glass,et al.  Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data , 2004, Heredity.

[36]  R. Frankham,et al.  Does Inbreeding and Loss of Genetic Diversity Decrease Disease Resistance? , 2004, Conservation Genetics.

[37]  M. Restani,et al.  SYLVATIC PLAGUE REDUCES GENETIC VARIABILITY IN BLACK-TAILED PRAIRIE DOGS , 2004, Journal of wildlife diseases.

[38]  S. Altizer,et al.  Rapid evolutionary dynamics and disease threats to biodiversity , 2003 .

[39]  S. Langevin,et al.  Experimental Infection of North American Birds with the New York 1999 Strain of West Nile Virus , 2003, Emerging infectious diseases.

[40]  L. Keller,et al.  Inbreeding effects in wild populations. , 2002 .

[41]  M. Beaumont,et al.  Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[42]  A. Kryukov,et al.  A Karyological Study of Some Corvine Birds (Corvidae, Aves) , 2001, Russian Journal of Genetics.

[43]  P. Donnelly,et al.  Association mapping in structured populations. , 2000, American journal of human genetics.

[44]  D. Coltman,et al.  PARASITE‐MEDIATED SELECTION AGAINST INBRED SOAY SHEEP IN A FREE‐LIVING ISLAND POPULATON , 1999, Evolution; international journal of organic evolution.

[45]  J M Cornuet,et al.  Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. , 1996, Genetics.

[46]  N. Freimer,et al.  Mutational processes of simple-sequence repeat loci in human populations. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[47]  S. O'Brien,et al.  Interactive influence of infectious disease and genetic diversity in natural populations , 1988, Trends in Ecology & Evolution.

[48]  M. Nei,et al.  THE BOTTLENECK EFFECT AND GENETIC VARIABILITY IN POPULATIONS , 1975, Evolution; international journal of organic evolution.

[49]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[50]  Menna E. Jones,et al.  Evidence that disease-induced population decline changes genetic structure and alters dispersal patterns in the Tasmanian devil , 2011, Heredity.

[51]  W. Babik,et al.  Collaboration for Environmental Evidence Systematic Review No . 65 DOES REDUCED MHC DIVERSITY DECREASE VIABILITY OF VERTEBRATE POPULATIONS ? , 2009 .

[52]  Claude-Alain H. Roten,et al.  Fast and accurate short read alignment with Burrows–Wheeler transform , 2009, Bioinform..

[53]  D. Robinson,et al.  EFFECTS OF WEST NILE VIRUS MORTALITY ON SOCIAL STRUCTURE OF AN AMERICAN CROW (CORVUS BRACHYRHYNCHOS) POPULATION IN UPSTATE NEW YORK , 2006 .

[54]  K. McGowan.  Demographic and behavioral comparisons of suburban and rural American Crows , 2001 .

[55]  L. Lim.  Introduction to Conservation Genetics , 2001 .

[56]  V. Loeschcke,et al.  Conservation Genetics , 2019, Handbook of Statistical Genomics.

[57]  S. Wright,et al.  Evolution in Mendelian Populations. , 1931, Genetics.