Speciation Through Evolution of Sex-Linked Genes

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Speciation Through Evolution of Sex-Linked Genes Heredity (2009) 102, 4–15 & 2009 Macmillan Publishers Limited All rights reserved 0018-067X/09 $32.00 www.nature.com/hdy SHORT REVIEW Speciation through evolution of sex-linked genes A Qvarnstro¨m and RI Bailey Department of Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Norbyva¨gen, Uppsala, Sweden Identification of genes involved in reproductive isolation expectation but mainly in female-heterogametic taxa. By opens novel ways to investigate links between stages of the contrast, there is clear evidence for both strong X- and speciation process. Are the genes coding for ecological Z-linkage of hybrid sterility and inviability at later stages of adaptations and sexual isolation the same that eventually speciation. Hence genes coding for sexual isolation traits are lead to hybrid sterility and inviability? We review the role of more likely to eventually cause hybrid sterility when they are sex-linked genes at different stages of speciation based on sex-linked. We conclude that the link between sexual four main differences between sex chromosomes and isolation and evolution of hybrid sterility is more intuitive in autosomes; (1) relative speed of evolution, (2) non-random male-heterogametic taxa because recessive sexually antag- accumulation of genes, (3) exposure of incompatible onistic genes are expected to quickly accumulate on the recessive genes in hybrids and (4) recombination rate. At X-chromosome. However, the broader range of sexual traits early stages of population divergence ecological differences that are expected to accumulate on the Z-chromosome may appear mainly determined by autosomal genes, but fast- facilitate adaptive speciation in female-heterogametic spe- evolving sex-linked genes are likely to play an important role cies by allowing male signals and female preferences to for the evolution of sexual isolation by coding for traits with remain in linkage disequilibrium despite periods of gene flow. sex-specific fitness effects (for example, primary and Heredity (2009) 102, 4–15; doi:10.1038/hdy.2008.93; secondary sexual traits). Empirical evidence supports this published online 10 September 2008 Keywords: speciation; sex-linkage; sexual selection; adaptation; genetic incompatibility; genetic mapping Introduction preferences or sperm-egg incompatibilities). Postzygotic isolation can be caused by extrinsic factors such as Understanding the speciation process remains a chal- inferior niche adaptation or reduced attractiveness of lenge in evolutionary biology (Coyne and Orr, 2004; hybrids or by intrinsic incompatibilities leading to Dieckmann et al., 2004; Price, 2007) but in recent decades reduced fertility or viability of hybrids. In general, much progress has been made regarding our knowledge closely related species are reproductively isolated be- of how reproductive isolation evolves. This focus on the cause of many different characteristics that have evolved evolution of reproductive isolation probably has its basis at different stages of their divergence. The build-up of in the biological species concept, which defines species as different forms of isolation often follow a temporal groups of organisms that are reproductively isolated pattern in which ecological differentiation and sexual from other such groups (Mayr, 1995). A species is then a isolation evolve rapidly and may often precede any form group of organisms that share the same gene pool. The of intrinsic genetic incompatibilities. Reduced fertility of rapid development of molecular tools has only recently hybrids then invariably precedes the rise of reduced made it possible to dive into those gene pools and viability. approach the process of speciation at the level of genes. Why do ecological and behavioural isolation tend to Studies identifying genes underlying reproductive isola- evolve quicker than intrinsic incompatibilities? Are the tion are starting to accumulate, opening up new genes coding for traits underlying ecological adaptations possibilities to answer central theoretical questions on and sexual isolation the same genes that eventually speciation. At the same time, this development causes become differentiated enough to cause hybrid sterility novel questions to arise. and inviability? Genomic studies have a clear role to play Reproductive isolation in sexually reproducing organ- in answering such central questions and also in revealing isms is caused by one or a combination of prezygotic and the underlying mechanisms behind general patterns of postzygotic isolation. Prezygotic isolation can be caused evolution of genetic incompatibilities such as Haldane’s by reduced probability of meeting (spatial or temporal rule. The nature of the genes underlying each form of isolation), mating (sexual isolation) or successful isolation may be intrinsically linked to their genomic fertilization (for example due to homogametic sperm distribution, and both are likely to affect the magnitude and chronology of their role in the speciation process. Correspondence: Associate Professor A Qvarnstro¨m, Department of Just as forms of isolation follow a temporal pattern, the Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, genetics of reproductive isolation may change through Norbyva¨gen 18D, SE-752 36 Uppsala, Sweden. time such that genes and genomic regions causing E-mail: [email protected] Received 8 February 2008; revised 16 July 2008; accepted 26 July isolation early in the speciation process may differ from 2008; published online 10 September 2008 those involved later on. Speciation and sex-linked genes A Qvarnstro¨m and RI Bailey 5 In this review we will ask whether genes causing mammals are unusual because all birds are female- reproductive isolation are often likely to be disproportio- heterogametic and all mammals male-heterogametic nately sex chromosome-linked and we will survey (Bull, 1983). This scattered taxonomic distribution and empirical studies to examine the level of support for the repeated evolution of sex chromosome systems (for the hypotheses of the association between sex linkage example, Charlesworth, 2002; Mank et al., 2006a) and of and speciation. The term ‘sex-linkage’ typically refers to male and female heterogamety should provide sufficient loci present on the sex chromosomes, which are defined statistical power for comparative analyses to examine as the chromosome pair that carries the constitutive their roles in speciation (for example, Mank et al., 2006b). genes controlling whether an individual develops into a male or a female (Box 1). Hence only organisms with separate sexes, as defined by the relative size of their Sex chromosomes and speciation gametes, have sex chromosomes. However, there are alternative mechanisms such as environmental sex Why expect sex-linked genes to have a disproportionately determination (for example, Sarre et al., 2004) or large influence on reproductive isolation? haplodiploidy, in which one sex is haploid and the other In the absence of differences in relevant features between diploid (for example, Hedrick and Parker, 1997). There sex chromosomes and autosomes, their influence on are also many species with genetic sex determination but speciation would be expected to be proportional to their with unidentified sex chromosomes (Ezaz et al., 2006; contribution to the genome in terms of size or the Mank et al., 2006a). The most widely known sex number of genes they carry (Ritchie and Phillips, 1998). chromosome systems are the XX/XY (females are However, there are at least four main factors that may homogametic and have two copies of the X chromosome lead to differences between sex chromosomes and whereas males are heterogametic and have one X and autosomes in their relationship with speciation, all of one Y) and ZZ/ZW (males have two Z chromosomes and which are linked to hemizygosity (Figure 1): (1) relative females have one Z and one W) systems. In general, the Y speed of evolution, (2) non-random accumulation of or W is smaller (Bull, 1983) and recombination between genes, (3) exposure of incompatible recessive genes in X/Z and Y/W chromosomes is often restricted to small hybrids and (4) recombination rate. Below we will regions. The fact that the X or Z is hemizygous in the discuss, in the light of different mechanisms of specia- heterogametic sex causes population genetic differences tion, whether components of reproductive isolation are between sex chromosomes and autosomes, and non- expected to be determined by sex-linked genes to a larger random accumulation of particular classes of genes on extent than is expected by chance. Our main aim is to sex chromosomes. These differences and their link to pinpoint how the four outlined differences between sex speciation will be discussed in this article. chromosomes and autosomes may influence the relative Chromosomal sex determination appears to have role of sex-linked genes at different stages of the evolved many times independently in both plants and speciation process. We focus on sex determination animals, with male heterogamety being more common. systems with stable heteromorphic sex chromosomes Insects, fishes, amphibians and reptiles contain a mix of and most of the following discussion will be of the X/Z male and female-heterogametic taxa, but birds and chromosome because it often contains more genes than Box 1 Sex chromosomes and sex determination The evolution of identifiable heteromorphic sex chromosomes is initiated by the spread of a sex-determining gene (SDG). This occurs when a new mutation
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