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. 2011 Feb;20(3):530-44.
doi: 10.1111/j.1365-294X.2010.04951.x. Epub 2010 Dec 24.

Identification of X-linked Quantitative Trait Loci Affecting Cold Tolerance in Drosophila Melanogaster and Fine Mapping by Selective Sweep Analysis

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Free PMC article

Identification of X-linked Quantitative Trait Loci Affecting Cold Tolerance in Drosophila Melanogaster and Fine Mapping by Selective Sweep Analysis

Nicolas Svetec et al. Mol Ecol. .
Free PMC article

Abstract

Drosophila melanogaster is a cosmopolitan species that colonizes a great variety of environments. One trait that shows abundant evidence for naturally segregating genetic variance in different populations of D. melanogaster is cold tolerance. Previous work has found quantitative trait loci (QTL) exclusively on the second and the third chromosomes. To gain insight into the genetic architecture of cold tolerance on the X chromosome and to compare the results with our analyses of selective sweeps, a mapping population was derived from a cross between substitution lines that solely differed in the origin of their X chromosome: one originates from a European inbred line and the other one from an African inbred line. We found a total of six QTL for cold tolerance factors on the X chromosome of D. melanogaster. Although the composite interval mapping revealed slightly different QTL profiles between sexes, a coherent model suggests that most QTL overlapped between sexes, and each explained around 5-14% of the genetic variance (which may be slightly overestimated). The allelic effects were largely additive, but we also detected two significant interactions. Taken together, this provides evidence for multiple QTL that are spread along the entire X chromosome and whose effects range from low to intermediate. One detected transgressive QTL influences cold tolerance in different ways for the two sexes. While females benefit from the European allele increasing their cold tolerance, males tend to do better with the African allele. Finally, using selective sweep mapping, the candidate gene CG16700 for cold tolerance colocalizing with a QTL was identified.

Conflict of interest statement

N.S. has special interest in the behavior, the genetics, and the life history of insects. A.W. works on QTL and selective sweep mapping in model organisms. R.W. works on adaptive consequences of standing genetic variation in natural populations, including humans. P.P. develops algorithms to detect selective sweeps in populations that have experienced past demographic changes. J.C. is focusing on theoretical models of genetic effects for improving quantitative analyses in general and QTL analyses in particular. K.B’s research interests include the characterization of meiotic recombination and the development of improved methods and software for QTL mapping. The main focus of D.M.’s research is on the development of model-based methods for the analysis of genetic data. W.S. works on various questions of theoretical and empirical population genetics (in particular adaptation).

Figures

Fig. 1
Fig. 1
Chill coma recovery curves of the parental lines (A* in black, E* in grey) separated for males (doted lines) and females (solid lines). Both males and females of the European line recovered significantly earlier from the chill coma than those of the African line (Welch’s t-test, P < 0.001). The black dotted horizontal line shows the time at which 50% of the line-specific flies recovered.
Fig. 2
Fig. 2
Mean ln[chill coma recovery time (CCRT)] in males (a) and females (b) of the X-chromosomal recombinant (XR) lines of Drosophila melanogaster. The smooth increase indicates multiple quantitative trait loci (QTL) with small to intermediate effects. Paternal cold tolerance (E*, grey triangle on the x-axis) as well as cold sensitivity (A*, black triangle) was not significantly higher in the males of the XR lines, whereas the females of one XR line showed a significantly shorter CCRT than the E* line (Welch’s t-test and Holm–Bonferroni correction, P < 0.05).
Fig. 3
Fig. 3
Results of interval-mapping methods for ln[chill coma recovery time (CCRT)] in males (a) and females (b) of Drosophila melanogaster. The one-quantitative trait loci (QTL) analysis (dotted lines) and the composite interval mapping (CIM) (solid lines) for males and females give consistent results, but the CIM better resolved the genetic architecture of multiple QTL for cold tolerance on the X chromosome. The horizontal lines correspond to the threshold values (dotted line for the one-QTL model and the solid one for the CIM). The distribution of the 23 genetic markers used is shown on the x-axis by triangles, where larger black triangles indicate the locations of QTL cofactors. Each position at which the LOD score exceeds the threshold value is a genomic region showing significant association with CCRT—i.e. a QTL.
Fig. 4
Fig. 4
Localization of quantitative trait loci (QTL)–sex interactions on the X chromosome of Drosophila melanogaster. The one-QTL analysis was sufficient to reveal a peak at 24.3 cM, which exceeds the 5% threshold of LOD = 1.79 (dotted line).
Fig. 5
Fig. 5
ln[chill coma recovery time (CCRT)] results in relation to the X-chromosomal recombinant (XR) line genotype at marker position 24 cM for males and females. While females significantly decrease their CCRT when having the European genotype at this marker position (Welch’s t-test, P < 0.001), males tend to increase their CCRT. However, the difference in CCRT between the males with European and African genotype was not significant. Such contrasting patterns for males and females are called quantitative trait loci (QTL)–sex interactions.
Fig. 6
Fig. 6
Profile of the ω statistic across the completely re-sequenced region of the European population. This 6.4-kb region consists of the intergenic fragment between the genes CG16700 and CG4991. The region shown on the x-axis is shorter than 6.4 kb because the genomic segment at the right end, between positions 5921 and 6379, was not included in the analysis because of smaller sample size (missing data). These positions correspond to the 3′UTR of CG4991. Likewise, positions containing indels were excluded. The dotted line represents the 5% significance level.

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