Sex chromosomes and speciation in Drosophila

Abstract

Two empirical rules suggest that sex chromosomes play a special role in speciation. The first is Haldane's rule-the preferential sterility and inviability of species hybrids of the heterogametic (XY) sex. The second is the disproportionately large effect of the X chromosome in genetic analyses of hybrid sterility. Whereas the causes of Haldane's rule are well established, the causes of the 'large X-effect' have remained controversial. New genetic analyses in Drosophila confirm that the X is a hotspot for hybrid male sterility factors, providing a proximate explanation for the large X-effect. Several other new findings-on faster X evolution, X chromosome meiotic drive, and the regulation of the X chromosome in the male-germline-provide plausible evolutionary explanations for the large X-effect. The two rules of speciation revisitedSpeciation-the process by which new biological species arise-corresponds to the evolution of reproductive barriers that limit the potential for genetic exchange between populations [1,2]. For geographically isolated populations, reproductive barriers evolve as incidental byproducts of genetic divergence. Eventually, 'good species' come to be completely isolated by one or more reproductive barriers that take the form of, e.g., incompatible courtship signals that prevent mating (prezygotic isolation) or incompatible gene interactions that cause the sterility or lethality of species hybrids (postzygotic isolation; Box 1). The past decade has seen good progress in the molecular characterization of the 'speciation genes' involved in reproductive barriers. In particular, the recent identification of genes causing intrinsic postzygotic isolation has begun to provide important information about the functions of these genes within species and on the population genetic forces that shape their evolutionary history [3,4]. I will not review the details of particular speciation genes here as they have been amply discussed elsewhere [3,4]. Instead, this review will focus on new developments that concern an older but still controversial problem-the special role of sex chromosomes in the evolution of postzygotic reproductive isolation between animal species.The idea that sex chromosomes play a special role in speciation is based on two empirical rules that characterize speciation in animals: Haldane's rule and the so-called 'large X-effect' [5,6]. Haldane's rule refers to the preferential sterility or inviability of species hybrids of the heterogametic (XY) sex: in crosses between many recently diverged species, XY hybrids are often sterile or inviable whereas their XX siblings are not [7]. In cases of unisexual hybrid sterility or inviability, Haldane's rule holds in 95% (n = 131) and 100% (n = 26) of species crosses in Drosophila and mammals, respectively, in which males are the XY sex, and in 97% (n = 87) and 96% (n = 114) of species crosses in birds and butterflies, respectively, in which dvnp@mail.rochester.edu, phone: (585) 275-8946, FAX: (585) 275-6066. Publisher's Disclaimer: This is a P...

Home-loving boreal hare mitochondria survived several invasions in Iberia: the relative roles of recurrent hybridisation and allele surfing

“…The four L. granatensis specimens and one L. europaeus with evidence of admixture were inferred to be backcrosses, suggesting that hybrids between these species are fertile, at least to a certain degree. However, no exchange could be detected for the sex chromosome markers, which may be an indication that they are implicated in hybrid unfitness, as is often the case (Presgraves, 2008). Even an X marker (Phka2), which had previously shown to have extensively introgressed from L. timidus into L. granatensis (Melo-Ferreira et al, 2011), did not show any evidence of gene flow from either L. timidus or L. granatensis into L. europaeus.…”

Patterns of Neutral Genetic Variation on Recombining Sex Chromosomes

“…Analyzing patterns in these polymorphisms could provide a new tool for studying a wide range of important evolutionary phenomena associated with sex chromosomes. These include speciation (Coyne and Orr 2004;Presgraves 2008), sex-antagonistic selection (Rice 1987;van Doorn and Kirkpatrick 2007), the evolution of recombination (Bergero and Charlesworth 2008), and meiotic drive (Presgraves 2008).…”

“…The chromosome region responsible for sex determination can shift frequently between different pairs of homologous chromosomes (Bull 1983;Mank et al 2006). Genes involved in isolation between species seem to be unusually common on sex chromosomes (Coyne and Orr 2004;Saetre et al 2007;Presgraves 2008). Sex chromosomes also appear to be enriched with genes for species-specific and secondary sexual traits [e.g., in lepidoptera (Prowell 1998), poeciliid fish (Lindholm and Breden 2002), and plants (Scotti and Delph 2006)].…”

Independent fusions and recent origins of sex chromosomes in the evolution and diversification of glass knife fishes (Eigenmannia)

“…This is likely to result in a significant level of infertility in potential F 1 hybrids because of abnormal meiotic segregation (Wallace et al, 2002). This effect would likely be compounded if the chromosome happened to harbor sex-determining genes, given the disproportionate importance of sex chromosomes in the evolution of post-mating isolation mechanisms (Presgraves, 2008;Kitano et al, 2009).…”