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The scope and strength of sex-specific selection in genome evolution.

Wright AE, Mank JE - J. Evol. Biol. (2013)

Bottom Line: Sex-specific selection is strongly influenced by mating system, which also causes neutral evolutionary changes that affect different regions of the genome in different ways.Here, we synthesize theoretical and molecular work in order to provide a cohesive view of the role of sex-specific selection and mating system in genome evolution.We also highlight the need for a combined approach, incorporating both genomic data and experimental phenotypic studies, in order to understand precisely how sex-specific selection drives evolutionary change across the genome.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Oxford, Edward Grey Institute, Oxford, UK. alison.e.wright@ucl.ac.uk

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Mating systems and effective population size (NE). Increasing differences between male and female reproductive success reduces NE (panel a), despite a constant overall population size. This difference between the sexes in reproductive success influences the NE of different portions of the genome in different ways (panel b). For autosomal genes, the largest effective population size (NEA) is seen when the variance in male and female reproductive success is equal; however, NEX and NEW increase with a greater proportion of females than males contributing to the next generation. The opposite is seen for NEZ and NEY, which are maximized when there are more males than females in the reproductive pool. This difference in the effect of mating system on the effective population size of different chromosomes makes contrasts between sex chromosomes and autosomes revealing (panel c).
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fig03: Mating systems and effective population size (NE). Increasing differences between male and female reproductive success reduces NE (panel a), despite a constant overall population size. This difference between the sexes in reproductive success influences the NE of different portions of the genome in different ways (panel b). For autosomal genes, the largest effective population size (NEA) is seen when the variance in male and female reproductive success is equal; however, NEX and NEW increase with a greater proportion of females than males contributing to the next generation. The opposite is seen for NEZ and NEY, which are maximized when there are more males than females in the reproductive pool. This difference in the effect of mating system on the effective population size of different chromosomes makes contrasts between sex chromosomes and autosomes revealing (panel c).

Mentions: Identifying signatures of genetic drift at the genetic level provides insight into the strength of neutral evolution. Mating systems define the variance in reproductive success between the sexes and thus the transmission of genetic material to subsequent generations, and the effect of mating system on the direction and rate of transmissions differs among regions of the genome. Although males and females share the autosomal portion of their genome equally, there is a pronounced asymmetry in the inheritance of the X chromosome (more often present in females), the Y chromosome (male-limited), the Z chromosome (more often present in males) and the W chromosome (female-limited). These inheritance patterns mean that different regions of the genome differ from each other in both their absolute effective populations size (NE), as well as their response in NE to differences in male and female mating success (Fig.3). Drift for autosomal loci is minimized in monogamous species compared to other mating systems, and deviations from monogamy will lead to elevated rates of genetic drift and decrease the efficacy of selection across the genome as a whole (Hartl & Clark, 2006). However, the relationship between drift and selection plays out differently on the sex chromosomes. The effective population size of both the X and Z chromosomes (NEX and NEZ) = ¾ that of the autosomes (NEA) in monogamous mating systems, creating a potential for increased genetic drift to act on homogametic sex chromosomes (Charlesworth et al., 1993; Vicoso & Charlesworth, 2009). Increased variance in male reproductive success associated with most forms of sexual selection increases NEX and decreases NEZ relative to NEA (Fig.3b–c); therefore, sexual selection on males is predicted to increase rates of neutral evolution for Z chromosomes more than X chromosomes, termed Faster-Z and Faster-X evolution (Mank et al., 2010c). This is supported by some evidence from birds (Mank et al., 2007, 2010b), mammals (Lau et al., 2009) and Drosophila (Connallon, 2007; Singh et al., 2007; Baines et al., 2008); however, other data are discordant with the role of mating sytem and sex chromosome evolution (Haddrill et al., 2010).


The scope and strength of sex-specific selection in genome evolution.

Wright AE, Mank JE - J. Evol. Biol. (2013)

Mating systems and effective population size (NE). Increasing differences between male and female reproductive success reduces NE (panel a), despite a constant overall population size. This difference between the sexes in reproductive success influences the NE of different portions of the genome in different ways (panel b). For autosomal genes, the largest effective population size (NEA) is seen when the variance in male and female reproductive success is equal; however, NEX and NEW increase with a greater proportion of females than males contributing to the next generation. The opposite is seen for NEZ and NEY, which are maximized when there are more males than females in the reproductive pool. This difference in the effect of mating system on the effective population size of different chromosomes makes contrasts between sex chromosomes and autosomes revealing (panel c).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4352339&req=5

fig03: Mating systems and effective population size (NE). Increasing differences between male and female reproductive success reduces NE (panel a), despite a constant overall population size. This difference between the sexes in reproductive success influences the NE of different portions of the genome in different ways (panel b). For autosomal genes, the largest effective population size (NEA) is seen when the variance in male and female reproductive success is equal; however, NEX and NEW increase with a greater proportion of females than males contributing to the next generation. The opposite is seen for NEZ and NEY, which are maximized when there are more males than females in the reproductive pool. This difference in the effect of mating system on the effective population size of different chromosomes makes contrasts between sex chromosomes and autosomes revealing (panel c).
Mentions: Identifying signatures of genetic drift at the genetic level provides insight into the strength of neutral evolution. Mating systems define the variance in reproductive success between the sexes and thus the transmission of genetic material to subsequent generations, and the effect of mating system on the direction and rate of transmissions differs among regions of the genome. Although males and females share the autosomal portion of their genome equally, there is a pronounced asymmetry in the inheritance of the X chromosome (more often present in females), the Y chromosome (male-limited), the Z chromosome (more often present in males) and the W chromosome (female-limited). These inheritance patterns mean that different regions of the genome differ from each other in both their absolute effective populations size (NE), as well as their response in NE to differences in male and female mating success (Fig.3). Drift for autosomal loci is minimized in monogamous species compared to other mating systems, and deviations from monogamy will lead to elevated rates of genetic drift and decrease the efficacy of selection across the genome as a whole (Hartl & Clark, 2006). However, the relationship between drift and selection plays out differently on the sex chromosomes. The effective population size of both the X and Z chromosomes (NEX and NEZ) = ¾ that of the autosomes (NEA) in monogamous mating systems, creating a potential for increased genetic drift to act on homogametic sex chromosomes (Charlesworth et al., 1993; Vicoso & Charlesworth, 2009). Increased variance in male reproductive success associated with most forms of sexual selection increases NEX and decreases NEZ relative to NEA (Fig.3b–c); therefore, sexual selection on males is predicted to increase rates of neutral evolution for Z chromosomes more than X chromosomes, termed Faster-Z and Faster-X evolution (Mank et al., 2010c). This is supported by some evidence from birds (Mank et al., 2007, 2010b), mammals (Lau et al., 2009) and Drosophila (Connallon, 2007; Singh et al., 2007; Baines et al., 2008); however, other data are discordant with the role of mating sytem and sex chromosome evolution (Haddrill et al., 2010).

Bottom Line: Sex-specific selection is strongly influenced by mating system, which also causes neutral evolutionary changes that affect different regions of the genome in different ways.Here, we synthesize theoretical and molecular work in order to provide a cohesive view of the role of sex-specific selection and mating system in genome evolution.We also highlight the need for a combined approach, incorporating both genomic data and experimental phenotypic studies, in order to understand precisely how sex-specific selection drives evolutionary change across the genome.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Oxford, Edward Grey Institute, Oxford, UK. alison.e.wright@ucl.ac.uk

Show MeSH