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Identification of a locus under complex positive selection in Drosophila simulans by haplotype mapping and composite-likelihood estimation - PubMed

Comparative Study

Identification of a locus under complex positive selection in Drosophila simulans by haplotype mapping and composite-likelihood estimation

Colin D Meiklejohn et al. Genetics. 2004 Sep.

Abstract

The recent action of positive selection is expected to influence patterns of intraspecific DNA sequence variation in chromosomal regions linked to the selected locus. These effects include decreased polymorphism, increased linkage disequilibrium, and an increased frequency of derived variants. These effects are all expected to dissipate with distance from the selected locus due to recombination. Therefore, in regions of high recombination, it should be possible to localize a target of selection to a relatively small interval. Previously described patterns of intraspecific variation in three tandemly arranged, testes-expressed genes (janusA, janusB, and ocnus) in Drosophila simulans included all three of these features. Here we expand the original sample and also survey nucleotide polymorphism at three neighboring loci. On the basis of recombination events between derived and ancestral alleles, we localize the target of selection to a 1.5-kb region surrounding janusB. A composite-likelihood-ratio test based on the spatial distribution and frequency of derived polymorphic variants corroborates this result and provides an estimate of the strength of selection. However, the data are difficult to reconcile with the simplest model of positive selection, whereas a new composite-likelihood method suggests that the data are better described by a model in which the selected allele has not yet gone to fixation.

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Figures

F<sc>igure</sc> 1.—
Figure 1.—

Diagram of the portion of chromosomal band 99D studied here. Solid bars represent exons and intervening lines represent introns. Bars above represent sequenced regions.

F<sc>igure</sc> 2.—
Figure 2.—

Sequence data for six genes in region 99D. The D. melanogaster (mel) sequence is from A

dams

et al. (2000); the D. yakuba (yak) sequences are from P

arsch

et al. (2001b)(janA-ocn) and C

accone

et al. (1996)(sryα). Asterisks below the sequences indicate nonsynonymous polymorphisms; vertical lines indicate noncoding polymorphisms. Boxed sites indicate that the rare D. simulans allele matches D. melanogaster and the common D. simulans allele matches D. yakuba; shaded sites indicate that the rare D. simulans allele matches D. yakuba and the common D. simulans allele matches D. melanogaster. Abbreviations for the location of origin of the D. simulans lines are: SA, South Africa; SM, St. Martin; JA, Japan; FR, France; TU, Tunisia; AU, Australia; HA, Haiti; US, United States; SE, Seychelles; PE, Peru; KE, Kenya; CO, Congo; PO, Polynesia; and ZI, Zimbabwe.

F<sc>igure</sc> 2.—
Figure 2.—

Sequence data for six genes in region 99D. The D. melanogaster (mel) sequence is from A

dams

et al. (2000); the D. yakuba (yak) sequences are from P

arsch

et al. (2001b)(janA-ocn) and C

accone

et al. (1996)(sryα). Asterisks below the sequences indicate nonsynonymous polymorphisms; vertical lines indicate noncoding polymorphisms. Boxed sites indicate that the rare D. simulans allele matches D. melanogaster and the common D. simulans allele matches D. yakuba; shaded sites indicate that the rare D. simulans allele matches D. yakuba and the common D. simulans allele matches D. melanogaster. Abbreviations for the location of origin of the D. simulans lines are: SA, South Africa; SM, St. Martin; JA, Japan; FR, France; TU, Tunisia; AU, Australia; HA, Haiti; US, United States; SE, Seychelles; PE, Peru; KE, Kenya; CO, Congo; PO, Polynesia; and ZI, Zimbabwe.

F<sc>igure</sc> 3.—
Figure 3.—

Low polymorphism and excess of singletons at janB. Graphs were generated using DnaSP 3.99 (R

ozas

et al. 2003) with a sliding window of 400 nucleotides and a step size of 25 nucleotides. (A) Average pairwise differences (T

ajima

1983) divided by divergence. (B) Fu and Li's D (F

u

and L

i

1993). The horizontal line indicates values of D that are significantly different from 0 at P < 0.05.

F<sc>igure</sc> 4.—
Figure 4.—

Parameter estimation for data sets simulated under incomplete sweep with α = 500, X = 6300, β = 0.7. (A) Joint distribution of X̂ and β̂. (B) Joint distribution of β̂ and α̂.

F<sc>igure</sc> 4.—
Figure 4.—

Parameter estimation for data sets simulated under incomplete sweep with α = 500, X = 6300, β = 0.7. (A) Joint distribution of X̂ and β̂. (B) Joint distribution of β̂ and α̂.

F<sc>igure</sc> 5.—
Figure 5.—

Average number of pairwise differences (π, solid line) and number of segregating sites (S, dashed line) for subsets of chromosomes that minimize π (πm(i)), graphed against the number of chromosomes in each subset. See text for details.

F<sc>igure</sc> 6.—
Figure 6.—

The composite-likelihood ratio (CLR) as a function of the position of the putative beneficial mutation. Sequenced segments corresponding to six genes in this region are indicated by horizontal lines above the x-axis. The CLR was obtained from 26 chromosomes corresponding to haplotype group I. The dashed line represents the 95th percentile of CLR (4.52) determined by neutral simulations.

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