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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

Mechanisms of mate choice influencing sexual isolation.Mate choice is any bias in male reproductive success caused by female responses (active or passive) to phenotypic differences between males (6; Text S1). The labelled female tissues (seminal receptacle not tested for overrepresentation of candidate mate choice genes; green  =  other untested parts of the reproductive tract) are possible locations for mechanisms of mate choice (bullet points). The arrows represent routes by which mate choice may occur. Active female choice is represented by arrows starting or finishing at the female brain; passive female choice by any arrows that do not involve the female brain. Arrows between tissues within the female represent neuronal and/or hormonal responses. The digestive tract, containing the majority of the remainder of the tested tissues, is represented in dark grey. ACPs  =  accessory gland proteins; CHCs  =  cuticular hydrocarbons.
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pone-0017358-g001: Mechanisms of mate choice influencing sexual isolation.Mate choice is any bias in male reproductive success caused by female responses (active or passive) to phenotypic differences between males (6; Text S1). The labelled female tissues (seminal receptacle not tested for overrepresentation of candidate mate choice genes; green  =  other untested parts of the reproductive tract) are possible locations for mechanisms of mate choice (bullet points). The arrows represent routes by which mate choice may occur. Active female choice is represented by arrows starting or finishing at the female brain; passive female choice by any arrows that do not involve the female brain. Arrows between tissues within the female represent neuronal and/or hormonal responses. The digestive tract, containing the majority of the remainder of the tested tissues, is represented in dark grey. ACPs  =  accessory gland proteins; CHCs  =  cuticular hydrocarbons.

Mentions: Biases in male reproductive success may be caused by multiple female choice components (Fig. 1; Text S1) that together can have an overriding influence on reproductive isolation between populations [8]. From a mechanistic point of view, female mate choice is the product of the interplay between neurological and physiological processes, which in turn are regulated by gene expression patterns during courtship and mating. An important step in understanding the link between mate choice and speciation is therefore to understand how female gene expression patterns affect reproductive isolation. Gene expression studies do not rely on pre-existing genetic divergence to reveal mechanistic associations between genes and traits, making them ideal for identifying genes that are potential targets for future divergence. Establishing the identity of the genes underlying plastic female responses to males belonging to their own population versus other populations can be used to make predictions of (i) the potential for future divergence, (ii) the rate by which divergence may proceed, and (iii) what evolutionary processes are likely to be driving their evolution.


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)

Mechanisms of mate choice influencing sexual isolation.Mate choice is any bias in male reproductive success caused by female responses (active or passive) to phenotypic differences between males (6; Text S1). The labelled female tissues (seminal receptacle not tested for overrepresentation of candidate mate choice genes; green  =  other untested parts of the reproductive tract) are possible locations for mechanisms of mate choice (bullet points). The arrows represent routes by which mate choice may occur. Active female choice is represented by arrows starting or finishing at the female brain; passive female choice by any arrows that do not involve the female brain. Arrows between tissues within the female represent neuronal and/or hormonal responses. The digestive tract, containing the majority of the remainder of the tested tissues, is represented in dark grey. ACPs  =  accessory gland proteins; CHCs  =  cuticular hydrocarbons.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0017358-g001: Mechanisms of mate choice influencing sexual isolation.Mate choice is any bias in male reproductive success caused by female responses (active or passive) to phenotypic differences between males (6; Text S1). The labelled female tissues (seminal receptacle not tested for overrepresentation of candidate mate choice genes; green  =  other untested parts of the reproductive tract) are possible locations for mechanisms of mate choice (bullet points). The arrows represent routes by which mate choice may occur. Active female choice is represented by arrows starting or finishing at the female brain; passive female choice by any arrows that do not involve the female brain. Arrows between tissues within the female represent neuronal and/or hormonal responses. The digestive tract, containing the majority of the remainder of the tested tissues, is represented in dark grey. ACPs  =  accessory gland proteins; CHCs  =  cuticular hydrocarbons.
Mentions: Biases in male reproductive success may be caused by multiple female choice components (Fig. 1; Text S1) that together can have an overriding influence on reproductive isolation between populations [8]. From a mechanistic point of view, female mate choice is the product of the interplay between neurological and physiological processes, which in turn are regulated by gene expression patterns during courtship and mating. An important step in understanding the link between mate choice and speciation is therefore to understand how female gene expression patterns affect reproductive isolation. Gene expression studies do not rely on pre-existing genetic divergence to reveal mechanistic associations between genes and traits, making them ideal for identifying genes that are potential targets for future divergence. Establishing the identity of the genes underlying plastic female responses to males belonging to their own population versus other populations can be used to make predictions of (i) the potential for future divergence, (ii) the rate by which divergence may proceed, and (iii) what evolutionary processes are likely to be driving their evolution.

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