Simpler mode of inheritance of transcriptional variation in male Drosophila melanogaster - PubMed (original) (raw)

Simpler mode of inheritance of transcriptional variation in male Drosophila melanogaster

Marta L Wayne et al. Proc Natl Acad Sci U S A. 2007.

Abstract

Sexual selection drives faster evolution in males. The X chromosome is potentially an important target for sexual selection, because hemizygosity in males permits accumulation of alleles, causing tradeoffs in fitness between sexes. Hemizygosity of the X could cause fundamentally different modes of inheritance between the sexes, with more additive variation in males and more nonadditive variation in females. Indeed, we find that genetic variation for the transcriptome is primarily additive in males but nonadditive in females. As expected, these differences are more pronounced on the X chromosome than the autosomes, but autosomal loci are also affected, possibly because of X-linked transcription factors. These differences may be of evolutionary significance because additive variation responds quickly to selection, whereas nonadditive genetic variation does not. Thus, hemizygosity of the X may underlie much of the faster male evolution of the transcriptome and potentially other phenotypes. Consistent with this prediction, genes that are additive in males and nonadditive in females are overrepresented among genes responding to selection for increased mating speed.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Percent variance explained for different components of genetic variation, plotted by sex. Blue squares represent genes on the X; black circles represent genes on the autosomes. Genes could be either significant for the particular term in one sex (males or females) or significant in both sexes (both significant). Plots are not presented for genes significant in SCA for males, for RGCA for females, or for RSCA for both sexes, because there were no significant genes in any of these categories.

Fig. 2.

Fig. 2.

A reciprocal cross: In the first cross, parent 1 (blue) is the sire, and parent 2 (red) is the dam; in the second, parent 2 (red) is the sire and parent 1 (blue) is the dam. Sons differ between pairs of reciprocal crosses for their single X chromosome, but daughters from both crosses are heterozygous for the X. Within each reciprocal cross, sons and daughters have identical cytoplasms but different X genotypes because sons are hemizygous, whereas daughters are heterozygous diploids. Reciprocal crosses also differ in both males and females for epigenetic and parent-of-origin effects, not illustrated here.

Fig. 3.

Fig. 3.

Each X chromosome from a female has an equal probability of being transmitted to a son or a daughter [red and orange Xs; the X from males is always transmitted to daughters, never to sons (blue X and arrow)].

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