The Contribution of Gene Movement to the “Two Rules of Speciation”

Abstract

The two "rules of speciation"-the Large X-effect and Haldane's rule-hold throughout the animal kingdom, but the underlying genetic mechanisms that cause them are still unclear. Two predominant explanations-the "dominance theory" and faster male evolution-both have some empirical support, suggesting that the genetic basis of these rules is likely multifarious. We revisit one historical explanation for these rules, based on dysfunctional genetic interactions involving genes recently moved between chromosomes. We suggest that gene movement specifically off or onto the X chromosome is another mechanism that could contribute to the two rules, especially as X chromosome movements can be subject to unique sex-specific and sex chromosome specific consequences in hybrids. Our hypothesis is supported by patterns emerging from comparative genomic data, including a strong bias in interchromosomal gene movements involving the X and an overrepresentation of male reproductive functions among chromosomally relocated genes. In addition, our model indicates that the contribution of gene movement to the two rules in any specific group will depend upon key developmental and reproductive parameters that are taxon specific. We provide several testable predictions that can be used to assess the importance of gene movement as a contributor to these rules in the future. K E Y W O R D S :Gene relocation, genomics, hybrid incompatibility, sterility, X chromosome.Interest in the genetic basis of speciation has exploded in the last few decades, fueled in large part by the application of new molecular genetic techniques to classical genetic studies of reproductive barriers between species (Coyne and Orr 2004). Much of this work-done in animal species with heterogametic sexdetermination-supports the existence of what have been called the "two rules of speciation" (Coyne and Orr 1989): the Large X-effect (the disproportionate influence of the X chromosome on the expression of interspecific hybrid incompatibility, particularly male sterility) and Haldane's rule (the observation that the heterogametic [XY or ZW] sex is disproportionately weaker or sterile in interspecific hybrids). Because of the prevalence of these patterns in a broad range of animal species (Coyne and Orr 2004), intense interest has focused on explaining their mechanistic basis, both with theoretical models (e.g., Orr and Turelli 2001) and emerging empirical data (e.g., Laurie 1997;Orr 1997;Masly and Presgraves 2007). These efforts have generated a set of plausible, often nonexclusive, explanations for the two patterns (Coyne and Orr 2004). However, disagreement remains over the predominant underlying genetic mechanism(s) responsible. The ubiquity of these patterns initially suggested that each might be due to a single common mechanism in heterogametic animal groups (Orr 1997). However, empirical support for several alternative hypotheses suggests that the genetic mechanisms contributing to these rules are likely multifarious (Orr 1993;Wu and Davis 1993;Coyne and Orr 2004). I...

Inferring the History of Interchromosomal Gene Transposition in Drosophila Using n-Dimensional Parsimony

“…Across all types of transpositions, we found that there was an overall excess of genes moving off the X chromosome (Table S9), consistent with previous findings (Betrán et al 2002;Bai et al 2007;Meisel et al 2009;Vibranovski et al 2009). However, there has been some disagreement about whether this pattern applies to all duplicates or just those formed by retrotransposition and how it varies between duplicative transpositions and relocations Meisel et al 2009;Vibranovski et al 2009;Moyle et al 2010;Zhang et al 2010). Our results contain the largest set of gene transpositions to date and should be able to provide a definitive answer.…”

“…However, this last study has been criticized on the grounds that too few instances of DNA-based transpositions were found for conclusive inference (Zhang et al 2010). The same patterns of movement are repeated in mammals, with an excess of X-to-autosome gene movements for RNA-based duplicative transpositions (Emerson et al 2004;Potrzebowski et al 2008) and for DNA-based relocations (Moyle et al 2010), but not for DNA-based duplications (Jiang et al 2007;). There are several hypotheses that attempt to explain the excess of Xto-autosome gene traffic, including sexually antagonistic selection (Rice 1984;Wu and Xu 2003;Connallon and Clark 2011), escape from X inactivation (Betrán et al 2002), meiotic drive (Meiklejohn and Tao 2010), and dosage compensation (Bachtrog et al 2010).…”

“…More recent studies have confirmed this excess of retrogenes moving off the X and neo-X chromosomes in multiple Drosophila species (Dai et al 2006;Bai et al 2007;Meisel et al 2009;Vibranovski et al 2009). Unlike retrogenes, DNA-based transpositions do not appear to consistently move in excess from the X to autosomes: while there is an excess found for DNAbased relocations in Drosophila (Bhutkar et al 2007;Meisel et al 2009;Vibranovski et al 2009;Moyle et al 2010), there is not an excess of DNA-based duplicative transpositions (Meisel et al 2009). However, this last study has been criticized on the grounds that too few instances of DNA-based transpositions were found for conclusive inference (Zhang et al 2010).…”

The Resolution of Sexual Antagonism by Gene Duplication

“…Duplication and differentiation between paralogs can alter the genetic architecture of male and female traits, and hybridization between species can potentially disrupt the transmission of sex-specific genes, leading to sex-specific hybrid inviability or sterility (see Lynch and Force 2000;Masly et al 2006). Gene duplication between chromosomes, particularly the movement of male functions from the X to the autosomes, can disproportionately affect males and might partially account for the two rules of speciation (Moyle et al 2010): ''Haldane's rule'' (Haldane 1922;Coyne and Orr 2004) and the ''large-X effect'' (Coyne and Orr 1989;True et al 1996;Tao et al 2003;Masly and Presgraves 2007;Presgraves 2008).…”

Haldane's rule in the 21st century

“…Among these, divergence of meiotic drive suppressor systems (Frank, 1991;Hurst and Pomiankowski, 1991;Tao andHartl, 2003 reviewed in McDermott andNoor, 2010) and other systems of genomic conflict (Johnson, 2010), inherent lability of spermatogenesis (Wu and Davis, 1993), faster X-chromosome evolution (Charlesworth et al, 1987) and Y chromosome and maternal effects (Sawamura, 1996;Turelli and Orr, 2000) have received most attention. In a recent paper, Moyle et al (2010) revisit the old, but largely neglected argument that intragenomic rearrangements may contribute to HR, and they present support for this in mammals, but not Drosophila.…”