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S Rule in the 21St Century Heredity (2011) 107, 95–102 & 2011 Macmillan Publishers Limited All rights reserved 0018-067X/11 www.nature.com/hdy REVIEW Haldane’s rule in the 21st century M Schilthuizen1,2, MCWG Giesbers2 and LW Beukeboom2 1Netherlands Centre for Biodiversity ‘Naturalis’, Leiden, The Netherlands and 2Evolutionary Genetics, Centre for Evolutionary and Ecological Studies, University of Groningen, Haren, The Netherlands Haldane’s Rule (HR), which states that ‘when in the offspring unambiguous novel results are rare. We further highlight how of two different animal races one sex is absent, rare, or research on organisms with sex determination systems sterile, that sex is the heterozygous (heterogametic) sex’, is different from those traditionally considered may lead to one of the most general patterns in speciation biology. We more insight in the underlying causes of HR. In particular, review the literature of the past 15 years and find that among haplodiploid organisms provide opportunities for testing the B85 new studies, many consider taxa that traditionally specific predictions of the dominance and faster X chromo- have not been the focus for HR investigations. The new some theory, and we present new data that show that studies increased to nine, the number of ‘phylogenetically the faster-male component of HR is supported in hermaph- independent’ groups that comply with HR. They continue to rodites, suggesting that genes involved in male function support the dominance and faster-male theories as explana- may evolve faster than those expressed in the female tions for HR, although due to increased reliance on indirect function. data (from, for example, differential introgression of cyto- Heredity (2011) 107, 95–102; doi:10.1038/hdy.2010.170; plasmic versus chromosomal loci in natural hybrid zones) published online 12 January 2011 Keywords: speciation genetics; hermaphrodites; haplodiploids; comparative studies; reproductive isolation; hybridization A short history this apparent generality, it came as a surprise when experimental studies in Drosophila revealed HR to be of a Haldane (1922) famously noticed that ‘when in the composite nature (Orr, 1993; Wu and Davis, 1993). Of the offspring of two different animal races one sex is absent, various composite modes that have been suggested for rare, or sterile, that sex is the heterozygous (hetero- the action of HR, there is strong support for two (the gametic) sex’. Haldane’s Rule (HR), as this observation dominance theory and the faster male theory), and has come to be known, has since been confirmed in many weaker support for some other modes (Coyne and Orr, groups of animals, including ones with male hetero- 2004 see below for details). gamety, such as Mammalia (mammals), Diptera (flies, mosquitoes and gnats), Orthoptera (grasshoppers and crickets), Teleostei (bony fish) and certain Amphibia Aims (amphibians), and with female heterogamety, such as Aves (birds), Lepidoptera (butterflies and moths) and Since its inception, literature on HR as well as reviews of certain Reptilia (reptiles) (Coyne, 1992; Laurie, 1997; Orr that literature have accumulated (Table 1). Whereas and Presgraves, 2000; Coyne and Orr, 2004; Volff, 2005; earlier reviews tended to aim for summaries of the Presgraves, 2010). As HR encompasses a generality taxonomic distribution and general support for the for the evolution of reproductive isolation, at least phenomenon (Craft, 1938; Laurie, 1997), later ones in gonochoric animals, it holds a central position in focused on evidence for the underlying genetic explana- speciation research, especially since the mid-1980s, when tions for HR (Orr, 1997), and by extension of speciation, studies of speciation genes began to blossom (Barton and and most recently on the actual genes that cause these Hewitt, 1985; Wu and Palopoli, 1994; Schilthuizen, 1999; incompatibilities (Presgraves, 2010; Johnson, 2010). In the Sun et al., 2004). Some debate has, however, centered past 15 years, attention has shifted towards traditionally around the correct measure for gauging the generality of less well-studied groups, such as Amphibia, Reptilia, HR: is the relevant measure the number of species pairs Teleostei and a number of invertebrate groups. These obeying HR or the number of independent sex determi- studies have not only expanded the taxonomic support nation systems in which it is found (Read and Nee, 1991). for HR, but have also offered interesting new insights Orr (1997) showed that, even if the latter criterion is and opportunities for testing theories underlying HR. applied, HR is generally adhered to: at least seven Complementing previous reviews (see Table 1), we phylogenetically independent origins are known. Given provide an update of species pairs tested for HR including some 85 studies published over the past 15 years (Table 2). We also tabulate evidence for the major Correspondence: Dr M Schilthuizen, NCB Naturalis, PO Box 9516, explanatory genetic theories (Tables 2 and 3). Consistent 2300 Leiden, The Netherlands. E-mail: [email protected] with previous reviews (Wu et al., 1996; Orr, 1997) this Received 2 July 2010; revised 12 November 2010; accepted 2 confirms the generality of the dominance theory, but also December 2010; published online 12 January 2011 suggests that alternative theories are often supported. Haldane’s rule in the 21st century M Schilthuizen et al 96 Table 1 Chronological overview of Haldane’s Rule literature reviews and their taxonomic foci Taxonomic group Reference Number of pairwise comparisons All taxa Haldane, 1922 6 Mammalia, 9 Aves, 30 Lepidoptera, 1 Diptera (Drosophila) Mammalia Craft, 1938 B30a Drosophila Coyne and Orr, 1989 145 (based on Bock, 1984) Mammalia Coyne and Orr, 1989 20 (based on Gray, 1954) Aves Coyne and Orr, 1989 43 (for fertility); 18 (for viability) (based on Gray, 1958) All taxa Coyne, 1992 25 Mammalia, 30 Aves, 36 Lepidoptera, 114 Diptera (Drosophila) All taxa Wu and Davis, 1993 25 Mammalia, 30 Aves, 36 Lepidopterab, 202 Diptera (Drosophila)c All taxa Laurie, 1997 25 Mammals, 30 Avesd, 1 Amphibia, 3 Reptilia, 196 Insecta (including 71 Lepidoptera), 1 Nematodae Aves Price and Bouvier, 2002 407 Anatinae (ducks) Tubaro and Lijtmaer, 2002 161 Columbidae (pigeons and doves) Lijtmaer et al., 2003 21 Lepidoptera Presgraves, 2002 212 Teleostei (bony fish) Russell, 2003 19 aSpecies status of some of the comparisons unclear. bSame data as in Coyne (1992). cCounting reciprocal crosses separately. dFrom Wu and Davis (1993). eSee Laurie (1997) for original references. Also, a relatively large number of studies (B20%) found taxonomic support for HR, making the number of patterns not predicted by HR. Such cases are chiefly phylogenetically independent supports larger. explained by postulating (or demonstrating) cytonuclear Supplementary Table 1 lists all known species tested incompatibilities (see below). Another goal of this review for HR since Laurie (1997) and expands Coyne and Orr’s is to draw attention to new taxonomic groups for (2004) table to 213 species pairs for sterility and 381 studying HR, in particular those which have both male species pairs for inviability, by the addition of 9 and female heterogamety in closely related taxa (for (sterility) þ 4 (inviability) Mammalia, 13 Drosophila (for example, Teleostei). Finally, we want to highlight the sterility), 3 þ 215 Aves, 6 þ 4 Lepidoptera, and newly, 66 potential of hitherto neglected animal groups with Amphibia (inviability), 1 Reptilia (inviability), 5 þ 6 alternative reproductive modes, such as hermaphrodites Teleostei and 4 þ 6 non-dipteran Insecta (Table 2). This and haplodiploids. We argue that these groups provide increases the number of phylogenetically independent unique opportunities to test specific predictions of supports for HR to nine (male-heterogametic fish and genetic theories underlying HR. male-heterogametic Gastropoda are added to the seven independently evolved sex determination systems with Taxonomic distribution HR already mentioned by Orr (1997)). These new taxa also throw a somewhat different light upon Orr’s (1997) Haldane (1922) provided the first broad taxonomic contention that heterogametic infertility would develop inventory of HR, tabulating Lepidoptera, Aves, Mamma- more easily than inviability in male-heterogametic taxa lia and one species pair of Diptera. Craft (1938) expanded whereas the reverse would be true for female-hetero- the list for Mammalia. After 50 years, Coyne and Orr gametic taxa. The new studies generally support this (1989) partly using data from Bock (1984) compiled the pattern, but the male-heterogametic Teleostei tend to list of Drosophila species, followed by Wu and Davis show the pattern usually encountered in female-hetero- (1993) partly based on data from Gray (1954, 1958), who gametic taxa. focused on Mammalia and Aves. Laurie (1997) provided a list of all taxa examined thus far. More recent authors Indirect evidence have focused in more detail on taxa with female heterogamety, viz Aves (Price and Bouvier, 2002; Tubaro The surge of interest in HR as part of the intensified and Lijtmaer, 2002; Lijtmaer et al., 2003), Lepidoptera speciation research of the past decades has led to (Presgraves, 2002) and certain Teleostei (Russell, 2003). increased familiarity with the phenomenon among The most recent update is by Coyne and Orr (2004) who students of non-model organisms. This has not only provide a summary table of the number of species that resulted in a taxonomically broader basis of case studies support HR. At that time,
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