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Female Drosophila melanogaster gene expression and mate choice: the X chromosome harbours candidate genes underlying sexual isolation.

Bailey RI, Innocenti P, Morrow EH, Friberg U, Qvarnström A - PLoS ONE (2011)

Bottom Line: We used mate choice experiments and gene expression analysis of female Drosophila melanogaster to examine three key components influencing speciation.Significant involvement of the brain and ovaries is consistent with the action of a combination of pre- and postcopulatory female choice mechanisms, while sex linkage and clustering of genes lead to high potential evolutionary rate and sheltering against the homogenizing effects of gene exchange between populations.Taken together our results imply favourable genomic conditions for the evolution of reproductive isolation through mate choice in Zimbabwean D. melanogaster and suggest that mate choice may, in general, act as an even more important engine of speciation than previously realized.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.

ABSTRACT

Background: The evolution of female choice mechanisms favouring males of their own kind is considered a crucial step during the early stages of speciation. However, although the genomics of mate choice may influence both the likelihood and speed of speciation, the identity and location of genes underlying assortative mating remain largely unknown.

Methods and findings: We used mate choice experiments and gene expression analysis of female Drosophila melanogaster to examine three key components influencing speciation. We show that the 1,498 genes in Zimbabwean female D. melanogaster whose expression levels differ when mating with more (Zimbabwean) versus less (Cosmopolitan strain) preferred males include many with high expression in the central nervous system and ovaries, are disproportionately X-linked and form a number of clusters with low recombination distance. Significant involvement of the brain and ovaries is consistent with the action of a combination of pre- and postcopulatory female choice mechanisms, while sex linkage and clustering of genes lead to high potential evolutionary rate and sheltering against the homogenizing effects of gene exchange between populations.

Conclusion: Taken together our results imply favourable genomic conditions for the evolution of reproductive isolation through mate choice in Zimbabwean D. melanogaster and suggest that mate choice may, in general, act as an even more important engine of speciation than previously realized.

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Related in: MedlinePlus

Non-random distribution of candidate mate choice genes.Significant clustering on the X chromosome is represented by pale blue, on the cytobands (1–100, shown on the labels beneath each chromosome) by medium blue, and on sub-bands (A–F, not labelled) by dark blue. There are a further 67 significant sub-sub-bands not represented (see Table S3).
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pone-0017358-g002: Non-random distribution of candidate mate choice genes.Significant clustering on the X chromosome is represented by pale blue, on the cytobands (1–100, shown on the labels beneath each chromosome) by medium blue, and on sub-bands (A–F, not labelled) by dark blue. There are a further 67 significant sub-sub-bands not represented (see Table S3).

Mentions: Traits associated with sexual isolation are predicted to be largely determined by sex-linked genes [4]. Existing QTL analyses using recombinant lines between ‘strong Z’ isofemale lines and M strain revealed that all chromosomes contribute to the stronger mate preferences of Z females compared to M. However, the strongest effects were on the autosomes, with a particularly strong effect of the tip of the left arm of chromosome III [21], [22]. In contrast to these previous studies, our study focuses on candidate genes underlying Z females overall responses to being courted and mated to males belonging to the Z or M lineages. We found that a disproportionately large number of our candidate mate choice genes were present on the X chromosome (Fig. 2; Table S3). If stronger discrimination were favoured by selection, the prediction based on this finding is more rapid future divergence than if the genes were spread evenly across chromosomes.


Female Drosophila melanogaster gene expression and mate choice: the X chromosome harbours candidate genes underlying sexual isolation.

Bailey RI, Innocenti P, Morrow EH, Friberg U, Qvarnström A - PLoS ONE (2011)

Non-random distribution of candidate mate choice genes.Significant clustering on the X chromosome is represented by pale blue, on the cytobands (1–100, shown on the labels beneath each chromosome) by medium blue, and on sub-bands (A–F, not labelled) by dark blue. There are a further 67 significant sub-sub-bands not represented (see Table S3).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3046225&req=5

pone-0017358-g002: Non-random distribution of candidate mate choice genes.Significant clustering on the X chromosome is represented by pale blue, on the cytobands (1–100, shown on the labels beneath each chromosome) by medium blue, and on sub-bands (A–F, not labelled) by dark blue. There are a further 67 significant sub-sub-bands not represented (see Table S3).
Mentions: Traits associated with sexual isolation are predicted to be largely determined by sex-linked genes [4]. Existing QTL analyses using recombinant lines between ‘strong Z’ isofemale lines and M strain revealed that all chromosomes contribute to the stronger mate preferences of Z females compared to M. However, the strongest effects were on the autosomes, with a particularly strong effect of the tip of the left arm of chromosome III [21], [22]. In contrast to these previous studies, our study focuses on candidate genes underlying Z females overall responses to being courted and mated to males belonging to the Z or M lineages. We found that a disproportionately large number of our candidate mate choice genes were present on the X chromosome (Fig. 2; Table S3). If stronger discrimination were favoured by selection, the prediction based on this finding is more rapid future divergence than if the genes were spread evenly across chromosomes.

Bottom Line: We used mate choice experiments and gene expression analysis of female Drosophila melanogaster to examine three key components influencing speciation.Significant involvement of the brain and ovaries is consistent with the action of a combination of pre- and postcopulatory female choice mechanisms, while sex linkage and clustering of genes lead to high potential evolutionary rate and sheltering against the homogenizing effects of gene exchange between populations.Taken together our results imply favourable genomic conditions for the evolution of reproductive isolation through mate choice in Zimbabwean D. melanogaster and suggest that mate choice may, in general, act as an even more important engine of speciation than previously realized.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.

ABSTRACT

Background: The evolution of female choice mechanisms favouring males of their own kind is considered a crucial step during the early stages of speciation. However, although the genomics of mate choice may influence both the likelihood and speed of speciation, the identity and location of genes underlying assortative mating remain largely unknown.

Methods and findings: We used mate choice experiments and gene expression analysis of female Drosophila melanogaster to examine three key components influencing speciation. We show that the 1,498 genes in Zimbabwean female D. melanogaster whose expression levels differ when mating with more (Zimbabwean) versus less (Cosmopolitan strain) preferred males include many with high expression in the central nervous system and ovaries, are disproportionately X-linked and form a number of clusters with low recombination distance. Significant involvement of the brain and ovaries is consistent with the action of a combination of pre- and postcopulatory female choice mechanisms, while sex linkage and clustering of genes lead to high potential evolutionary rate and sheltering against the homogenizing effects of gene exchange between populations.

Conclusion: Taken together our results imply favourable genomic conditions for the evolution of reproductive isolation through mate choice in Zimbabwean D. melanogaster and suggest that mate choice may, in general, act as an even more important engine of speciation than previously realized.

Show MeSH
Related in: MedlinePlus