Population Genomics: Whole-Genome Analysis of Polymorphism and Divergence in Drosophila simulans

Begun, David J.; Holloway, Alisha K.; Stevens, Kristian; Hillier, La Deana W.; Poh, Yu Ping; Hahn, Matthew W.; Nista, Phillip M.; Jones, Corbin D.; Kern, Andrew D.; Dewey, Colin N.; Pachter, Lior; Myers, Eugene W.; Langley, Charles H.

doi:10.1371/journal.pbio.0050310

Cited by 607 publications

(900 citation statements)

References 139 publications

Supporting

Mentioning

817

Contrasting

Order By: Relevance

“…This is a very small number indeed, equivalent to a single recent sweep affecting ,1% of all genes. Indeed in Drosophila the fraction of loci affected by recent positive selection may be quite large (Begun et al 2007;Langley et al 2012). Numerous studies have estimated that the fraction of adaptive amino acid substitutions in D. melanogaster is considerable, with estimates ranging from 10 to 50% (Smith and EyreWalker 2002;Bierne and Eyre-Walker 2004;Langley et al 2012;Mackay et al 2012).…”

Section: Discussionmentioning

confidence: 99%

Effects of Linked Selective Sweeps on Demographic Inference and Model Selection

2016

Self Cite

View full text Add to dashboard Cite

The availability of large-scale population genomic sequence data has resulted in an explosion in efforts to infer the demographic histories of natural populations across a broad range of organisms. As demographic events alter coalescent genealogies, they leave detectable signatures in patterns of genetic variation within and between populations. Accordingly, a variety of approaches have been designed to leverage population genetic data to uncover the footprints of demographic change in the genome. The vast majority of these methods make the simplifying assumption that the measures of genetic variation used as their input are unaffected by natural selection. However, natural selection can dramatically skew patterns of variation not only at selected sites, but at linked, neutral loci as well. Here we assess the impact of recent positive selection on demographic inference by characterizing the performance of three popular methods through extensive simulation of data sets with varying numbers of linked selective sweeps. In particular, we examined three different demographic models relevant to a number of species, finding that positive selection can bias parameter estimates of each of these models-often severely. We find that selection can lead to incorrect inferences of population size changes when none have occurred. Moreover, we show that linked selection can lead to incorrect demographic model selection, when multiple demographic scenarios are compared. We argue that natural populations may experience the amount of recent positive selection required to skew inferences. These results suggest that demographic studies conducted in many species to date may have exaggerated the extent and frequency of population size changes.KEYWORDS population genetics; positive selection; demographic inference T HE widespread availability of population genomic data has spurred a new generation of studies aimed at understanding the histories of natural populations from a host of model and nonmodel organisms alike. In particular, genomescale variation data allows for inference of demographic factors such as population size changes, the timing and ordering of population splits, migration rates between populations, and the founding of admixed populations (Pool et al. 2010;Pickrell and Pritchard 2012;Sousa and Hey 2013). Such efforts can refine our picture of demographic events inferred from the archaeological record (e.g., Fagundes et al. 2007;Goebel et al. 2008), or reveal such events in species where no archaeological data are available, and can aid conservation efforts by complementing census data (e.g., Hájková et al. 2007;Garrick et al. 2015).Population genomic data sets are well suited for this task simply because demographic changes leave their mark on patterns of genetic variation. Recent population growth, for example, will result in an excess of rare variation compared to equilibrium expectations (Fu 1997), while population contraction will result in an excess of intermediate frequency alleles (Maruyama and Fuerst 198...

show abstract

Section: Discussionmentioning

confidence: 99%

Effects of Linked Selective Sweeps on Demographic Inference and Model Selection

2016

Self Cite

View full text Add to dashboard Cite

show abstract

“…In several Drosophila species, nucleotide diversity differs by B10-fold between regions of high and low recombination (Stephan et al, 1992;Aquadro et al, 1994;Begun et al, 2007). Selective sweeps and/or background selection could account for these results.…”

Section: Low Genetic Diversity In Regions With Low Recombination Ratesmentioning

confidence: 99%

How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination

Frankham

2011

Heredity

View full text Add to dashboard Cite

Levels of genetic diversity in finite populations are crucial in conservation and evolutionary biology. Genetic diversity is required for populations to evolve and its loss is related to inbreeding in random mating populations, and thus to reduced population fitness and increased extinction risk. Neutral theory is widely used to predict levels of genetic diversity. I review levels of genetic diversity in finite populations in relation to predictions of neutral theory. Positive associations between genetic diversity and population size, as predicted by neutral theory, are observed for microsatellites, allozymes, quantitative genetic variation and usually for mitochondrial DNA (mtDNA). However, there are frequently significant deviations from neutral theory owing to indirect selection at linked loci caused by balancing selection, selective sweeps and background selection. Substantially lower genetic diversity than predicted under neutrality was found for chromosomes with low recombination rates and high linkage disequilibrium (compared with 'normally' recombining chromosomes within species and adjusted for different copy numbers and mutation rates), including W (median 100% lower) and Y (89% lower) chromosomes, dot fourth chromosomes in Drosophila (94% lower) and mtDNA (67% lower). Further, microsatellite genetic and allelic diversity were lost at 12 and 33% faster rates than expected in populations adapting to captivity, owing to widespread selective sweeps. Overall, neither neutral theory nor most versions of the genetic draft hypothesis are compatible with all empirical results.

show abstract

“…Another concern is the possibility of phylogenetic relationships being confounded by the repeated introgression of mtDNA. To a certain degree, the same pitfalls apply to nuclear genes and because of these complications, many recent studies use a multi-locus, multigenome or whole-genome approach to avoid biased phylogenetic inference from single-gene data (Begun et al, 2007;Nazari et al, 2007;Winterton et al, 2007;Regier et al, 2008). Such a multi-locus strategy does not work for mtDNA as it is inherited as a single linkage group.…”

Section: Discussionmentioning

confidence: 99%

Introgression as a likely cause of mtDNA paraphyly in two allopatric skippers (Lepidoptera: Hesperiidae)

et al. 2009

View full text Add to dashboard Cite

Gene transfer between species during interspecific hybridization is a widely accepted reality in plants but is considered a relatively rare phenomenon among animals. Here we describe a unique case of mitochondrial DNA (mtDNA) paraphyly in the skipper genus, Erynnis, that involves well-diverged allopatric species. Using molecular evidence from both mitochondrial and nuclear genomes, we found high levels of intraspecific divergence in the mitochondrial genome within E. propertius (over 4% pair-wise sequence divergence) but no such differentiation in the nuclear genome. Sequence comparisons with related Erynnis suggest that past, but recent and infrequent introgression between E. propertius and E. horatius is the most reasonable explanation for the observed pattern of mtDNA paraphyly. This example of putative introgression highlights the complexity of mtDNA evolution and suggests that similar processes could be operating in other taxa that have not been extensively sampled. Our observations reinforce the importance of involving multiple genes with different modes of inheritance in the analysis of population history of congeneric taxa.

show abstract

Population Genomics: Whole-Genome Analysis of Polymorphism and Divergence in Drosophila simulans

Cited by 607 publications

References 139 publications

Effects of Linked Selective Sweeps on Demographic Inference and Model Selection

Effects of Linked Selective Sweeps on Demographic Inference and Model Selection

How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination

Introgression as a likely cause of mtDNA paraphyly in two allopatric skippers (Lepidoptera: Hesperiidae)

Contact Info

Product

Resources

About