Sex‐specific recombination rates in Parus major and P. caeruleus, an exception to Huxley's rule

摘要

“It appears to be a general rule that wherever crossing-over is absent or markedly reduced in one sex, that sex is the heterogametic sex” (Huxley 1928). However, already six years earlier Haldane (1922) stated in his study on sex-specific differences in recombination frequency in hybrids of animal species “When in the F1 offspring of two different animal races one sex is absent, rare or sterile, that sex is the heterozygous sex”. One explanation for this phenomenon given by Haldane (1922) was close linkage of sex-linked factors due to a greater difficulty of fusion of chromosome pairs in the heterogametic sex. In addition to interspecific processes such as speciation Haldane's rule, therefore, has been also cited in subsequently published literature to explain intraspecific mechanisms such as the interference of recombination in the evolution of sex chromosomes. Accordingly, higher recombination rates in human females than in males, for example, were accepted as being in line with Haldane's rule (Ott 1988; Strachan and Read 1996). However, as long as evolutionary mechanisms are unknown that led Haldane (1922) and Huxley (1928) to put forward their rules, we will follow Dunn and Bennett (1967) and distinguish between two rules: i.e. Haldane's rule for the sex ratio and sterility differences in hybrids, and Huxley's rule for intraspecific differences in recombination rates.There are numerous experimental and theoretical studies aimed at assessing the general validity of Haldane's rule (reviewed by Laurie 1997). Hybridization studies of various insect and bird species provide strong support for Haldane's rule (Coyne 1985, 1992; Wu and Davis 1993, Wu et al. 1996). Beyond this, there is wide compliance with the rule across phylogenetic boundaries and additional examples are given for amphibians (Bull 1983; Rykena 1991) and the nematode Caenorhabditis (Baird et al. 1992). In the context with Haldane's rule, theoretical studies have assessed genetic mechanisms that may be responsible for the postzygotic isolation of species during speciation processes. The recessivity of incompatibilities has been proposed to be the basis for Haldane's rule (Muller 1942). Muller's dominance theory is also strongly supported by mathematical studies (Turelli and Orr 1995, 2000; Orr and Turelli 1996; Turelli and Begun 1997). However, some studies on Drosophila (D. simulans and D. melanogaster) and Lepidoptera species (Heliothis species) yielded data that are incompatible with Haldane's rule. These Drosophila cases are regarded as an exception to Haldane's rule because of cytoplasmatic or maternal zygotic incompatibilities (Sawamura et al. 1993a,b; Sawamura 1996). In interspecific crosses between the Lepidoptera species Heliothis virescens and H. subflexa, a fitness loss of hybrids was found for both sexes; homogametic males were sterile and heterogametic females had only reduced fecundity or fertility (Proshold and LaChance 1974). Regardless of exceptions Haldane's rule requires reproductive isolation during speciation which is enforced by anti-recombinational mechanisms (Forsdyke 1995, 1996).The general validity of Huxley's rule has been discussed as well. Soon after publication of Huxley's rule, some authors noticed exceptions to the rule when studying morphological traits and recombination in birds. Colour inheritance in the domestic pigeon, for example, indicated higher recombination frequencies in females than in males (Hollander 1938). Higher recombination rates in the heterogametic sex were also demonstrated in fowls for several linkage groups (Landauer 1933; Fisher and Landauer 1953). There is a large number of publications discussing the general validity of Huxley's rule in numerous species. Surprisingly, none of those compares recombination processes for the same set of loci in closely related species. Such an approach, however, can provide a more detailed insight in the validity of the rule. Therefore, we tested the linkage between 12 loci in