Detecting past population bottlenecks using temporal genetic data

Population bottlenecks wield a powerful influence on the evolution of species and populations by reducing the repertoire of responses available for stochastic environmental events. Although modern contractions of wild populations due to human‐related impacts have been documented globally, discerning historic bottlenecks for all but the most recent and severe events remains a serious challenge. Genetic samples dating to different points in time may provide a solution in some cases. We conducted serial coalescent simulations to assess the extent to which temporal genetic data are informative regarding population bottlenecks. These simulations demonstrated that the power to reject a constant population size hypothesis using both ancient and modern genetic data is almost always higher than that based solely on modern data. The difference in power between the modern and temporal DNA approaches depends significantly on effective population size and bottleneck intensity and less significantly on sample size. The temporal approach provides more power in cases of genetic recovery (via migration) from a bottleneck than in cases of demographic recovery (via population growth). Choice of genetic region is critical, as mutation rate heavily influences the extent to which temporal sampling yields novel information regarding the demographic history of populations.

[1]  Jon A Yamato,et al.  Maximum likelihood estimation of population growth rates based on the coalescent. , 1998, Genetics.

[2]  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.

[3]  Craig R. Miller,et al.  The history of effective population size and genetic diversity in the Yellowstone grizzly (Ursus arctos): Implications for conservation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[5]  Christian N. K. Anderson,et al.  Serial SimCoal: A population genetics model for data from multiple populations and points in time , 2005, Bioinform..

[6]  H. Harpending,et al.  Population growth makes waves in the distribution of pairwise genetic differences. , 1992, Molecular biology and evolution.

[7]  S. O’Brien,et al.  Elephant seal genetic variation and the use of simulation models to investigate historical population bottlenecks. , 1993, The Journal of heredity.

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

[9]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[10]  Jinyan Li,et al.  Twelve C2H2 zinc-finger genes on human chromosome 19 can be each translated into the same type of protein after frameshifts , 2004, Bioinform..

[11]  E. Hadly,et al.  ANCIENT DNA EVIDENCE OF PROLONGED POPULATION PERSISTENCE WITH NEGLIGIBLE GENETIC DIVERSITY IN AN ENDEMIC TUCO-TUCO (CTENOMYS SOCIABILIS) , 2003 .

[12]  R. Wayne,et al.  Genetic variation of microsatellite loci in a bottlenecked species: the northern hairy‐nosed wombat Lasiorhinus krefftii , 1994, Molecular ecology.

[13]  J. Cook,et al.  MtDNA Evidence for Repeated Pulses of Speciation Within Arvicoline and Murid Rodents , 1999, Journal of Mammalian Evolution.

[14]  R. Wayne,et al.  A genetic record of population isolation in pocket gophers during Holocene climatic change. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[15]  W. Brown,et al.  Rapid evolution of animal mitochondrial DNA. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[16]  G. Luikart,et al.  Distortion of allele frequency distributions provides a test for recent population bottlenecks. , 1998, The Journal of heredity.

[17]  S. Pääbo,et al.  Lack of phylogeography in European mammals before the last glaciation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  B. Charlesworth,et al.  Genetic Revolutions, Founder Effects, and Speciation , 1984 .

[19]  Jon A Yamato,et al.  Estimating effective population size and mutation rate from sequence data using Metropolis-Hastings sampling. , 1995, Genetics.

[20]  C. Gissi,et al.  Nucleotide Substitution Rate of Mammalian Mitochondrial Genomes , 1999, Journal of Molecular Evolution.

[21]  R. Slade Molecular population genetics of the southern elephant seal , 1995 .

[22]  C. Moritz,et al.  Molecular population genetics of the southern elephant seal Mirounga leonina. , 1998, Genetics.

[23]  M. Nordborg,et al.  Coalescent Theory , 2019, Handbook of Statistical Genomics.

[24]  R. Wayne,et al.  Population genetics of ice age brown bears. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. Beaumont Estimation of population growth or decline in genetically monitored populations. , 2003, Genetics.

[26]  Uma Ramakrishnan,et al.  Genetic Response to Climatic Change: Insights from Ancient DNA and Phylochronology , 2004, PLoS biology.

[27]  N. Lehman,et al.  Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendi). , 2004, The Journal of heredity.

[28]  L. Excoffier,et al.  Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. , 1999, Genetics.

[29]  Jean-Marie Cornuet,et al.  Likelihood-based estimation of the effective population size using temporal changes in allele frequencies: a genealogical approach. , 2002, Genetics.

[30]  R. Waples A generalized approach for estimating effective population size from temporal changes in allele frequency. , 1989, Genetics.

[31]  J. Garza,et al.  Detection of reduction in population size using data from microsatellite loci , 2001, Molecular ecology.

[32]  R. Frankham,et al.  Rapid genetic deterioration in captive populations: Causes and conservation implications , 2002, Conservation Genetics.

[33]  K. Kidd,et al.  Modern African ape populations as genetic and demographic models of the last common ancestor of humans, chimpanzees, and gorillas. , 2001, The Journal of heredity.

[34]  Robert C. Lacy,et al.  Importance of Genetic Variation to the Viability of Mammalian Populations , 1997 .

[35]  D. H. Reed,et al.  Inbreeding and extinction: The effect of environmental stress and lineage , 2002, Conservation Genetics.

[36]  M. Slatkin,et al.  Using maximum likelihood to estimate population size from temporal changes in allele frequencies. , 1999, Genetics.

[37]  E. Thompson,et al.  Monte Carlo evaluation of the likelihood for N(e) from temporally spaced samples. , 2000, Genetics.

[38]  M W Bruford,et al.  Inbreeding of bottlenecked butterfly populations. Estimation using the likelihood of changes in marker allele frequencies. , 1999, Genetics.

[39]  C. Millar,et al.  Rates of Evolution in Ancient DNA from Adélie Penguins , 2002, Science.

[40]  G. Spong,et al.  High genetic variation in leopards indicates large and long‐term stable effective population size , 2000, Molecular ecology.

[41]  G. A. Horridge,et al.  Animal species and evolution. , 1964 .

[42]  Alexei J Drummond,et al.  Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. , 2002, Genetics.

[43]  M. Nei,et al.  Gene genealogy and variance of interpopulational nucleotide differences. , 1985, Genetics.

[44]  M. Slatkin In Defense of Founder-Flush Theories of Speciation , 1996, The American Naturalist.

[45]  A. von Haeseler,et al.  Pattern of nucleotide substitution and rate heterogeneity in the hypervariable regions I and II of human mtDNA. , 1999, Genetics.

[46]  J. Wang,et al.  A pseudo-likelihood method for estimating effective population size from temporally spaced samples. , 2001, Genetical research.

[47]  J. Searle,et al.  Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences , 2002, Molecular ecology.