Introduction
Sex differences in recombination were discovered in the first linkage studies on Drosophila [1,2] and Bombyx (Tanaka [1914] in [3]) almost one century ago. However, this observation remains today largely unexplained despite several attempts. Based on very limited observations (see Table 1), especially of Bombyx, in which the female is heterogametic, Haldane [3] suggested, as far as “these facts are anything more than a coincidence,” that the lower autosomal recombination rate in the heterogametic sex may reflect a pleiotropic consequence of selection against recombination between the sex chromosomes. Later, Huxley [4] showed that Gammarus males also recombined less than females. He gave the same evolutionary explanation, although he restricted it to cases of a marked sex difference.
Table 1  Data on Which the Haldane-Huxley Rule is Based
Listed are the data available to Haldane [4] when he proposed the Haldane-Huxley rule
a  rm represents recombination in males
b  rf represents recombination in females
c Plus and minus symbols indicate the direction of heterochiasmy, and zero indicates achiasmy This conjecture has now been confirmed for achiasmate species (i.e., species in which only one sex recombines) and is referred to as Haldane-Huxley rule: Nei [5] showed theoretically that tight linkage should evolve on Y or W chromosomes, and Bell [6] compiled a large dataset showing that achiasmy evolved 29–34 times independently, each time with no recombination in the heterogametic sex.
However, for heterochiasmate species, three problems with the Haldane-Huxley pleiotropy explanation were discovered [7,8]. The first problem arose when substantial variation in male-female differences in recombination rate was found between pairs of autosomes within mice [8] and Tribolium [9,10], and between genotypes for the same pair of autosomes [11]. The second problem was the discovery that hermaphrodite species (the platyhelminth Dendrocoelum [12] and the plant Allium [13]) may present strong heterochiasmy between male and female meiosis despite having no sex chromosomes or even sex-determining loci. The third problem was the discovery of species in which the heterogametic sex recombines more than the homogametic one (e.g., in some Triturus species) [14]. Because of these contradictory observations, variation in heterochiasmy has remained difficult to explain because of the absence of an alternative theory as well as the lack of a clear pattern in the data.
In 1969, Nei [5] worked out the first “modifier” model to study the evolution of sex differences in recombination, and concluded for autosomes that “the evolutionary mechanism of these sex differences is not known at present.” Surveying an updated dataset, Bell [6] concluded that “female gametes experience more crossing over among hermaphroditic plants (and perhaps animals), but this is not invariably the case among gonochoric animals (…) certainly (this) has never received any explanation.” The idea that heterochiasmy may be explained by a sex rather than by a sex chromosome effect, which was ignored by Haldane because of Bombyx, was reconsidered. This led Trivers [15] to suggest that, because only males with very good gene combinations reproduce (relative to females, for whom reproduction success is often less variable), they should recombine less to keep intact these combinations. He accounted for exceptions by variation in the regime of sexual selection. The idea was criticized by Burt et al. [16], who also questioned the correlations—with an updated dataset—between heterochiasmy and either sex or heterogamety. These authors tried to correlate the level of heterochiasmy with the amount of “opportunity for sex-specific selection,” but failed to find an effect. They were tempted to advocate neutrality, but were puzzled by the positive correlation between male and female recombination rate and by evidence showing compensation (e.g., female mice tend to recombine more on the X, as if they were compensating for no recombination in males; similarly, no species is known with achiasmy in both sexes [16]). In 1994, Korol et al. [17] insisted on a possible role for gametic selection but did not give evidence in favour of this claim. Recently, Lenormand [18], using Nei's modifier approach, showed that it is very difficult to explain heterochiasmy by sex-specific diploid selection. Rather, a sex difference in selection during haploid phase, or a sex difference in diploid selection on imprinted genes, is a more likely explanation. He predicted that, as far as haploid selection is concerned, the sex experiencing the more intense haploid selection should recombine less. Indeed, when allelic effects interact to determine fitness (i.e., when there is “epistasis,” either negative or positive), recombining decreases mean fitness in the population of the next generation [19]. This effect occurs because recombination breaks up combinations of genes that have previously been built up by selection. For a given average recombination rate between sexes and for a given average epistasis between male and female haploids, it is always advantageous for the haploid population (male or female) with the greatest absolute value in epistasis to be produced with the lowest amount of recombination. In this way, the “recombination load” that the haploid population is exposed to is minimized.
In this paper, we would like to come up with a more quantitative evaluation of the possible role of haploid selection in shaping heterochiasmy. For that purpose, we first updated the dataset of Burt et al. [16] on heterochiasmy, focusing on genetic maps that have become available over the last 15 years. We then determined how fast heterochiasmy evolves, in order to measure the amount of phylogenetic inertia on this trait. Finally, we determined whether variables such as gender, heterogamety, or the opportunity for selection in the haploid phase, could explain variation in heterochiasmy. If there is selection with substantial epistasis on some genes during the haploid phase, we expect the sex with the greater opportunity for haploid selection to show less recombination. Alternatively, if selection during the haploid phase is weak or without substantial epistasis, we do not expect it to produce a directional bias in the amount of recombination displayed by either sex.