Results/Discussion

Sex Chromosomes
Heterochiasmy is a fast-evolving trait, and phylogenetic inertia does not satisfactorily explain its distribution. In contrast to achiasmy, we found that heterochiasmy is not influenced by the nature of the sex chromosomes. This is interesting, because it suggests that achiasmy and heterochiasmy are influenced by qualitatively different evolutionary forces, although they seem to differ only quantitatively. It would be useful to determine whether achiasmy evolved to reduce the average recombination rate or to change the relative amount of recombination between the sexes. The two situations may be discriminated by determining whether the homogametic sex in achiasmate species tends to recombine more than in closely related chiasmate species. Evidence for such compensation would indicate that achiasmy did not evolve to reduce the average recombination rate. In the absence of such compensation, however, achiasmy may simply reflect selection for tight linkage. In such a situation, we propose that Haldane-Huxley rule may be caused by the converse argument to the one previously considered: The presence of achiasmy only in the heterogametic sex may reflect selection to maintain nonzero recombination rate on X or Z chromosomes in the homogametic sex. In species in which the average autosomal recombination rate is selected against (i.e., towards a lower equilibrium value), loss-of-function (recombination) mutations with an effect restricted to one sex may spread only if they affect the heterogametic sex, because mutations suppressing recombination in the homogametic sex completely suppress recombination on the X or Z chromosome. The same argument applies to XO species and may explain why achiasmy is associated only with the heterogametic sex. In addition, this hypothesis does not require the existence of genes suppressing recombination between the sex chromosomes with autosomal pleiotropic effects. Under this hypothesis, there is no reason to find an effect of the presence of heteromorphic sex chromosome on the amount of heterochiasmy, as originally envisioned by Haldane and Huxley. Overall, this hypothesis would explain why heterochiasmy and achiasmy differ qualitatively and why we do not observe any effect of sex chromosomes on heterochiasmy.

Heterochiasmy in Animals
In animals, male-female dimorphism in haploid selection may also contribute to heterochiasmy. In general, there is no female haploid phase in animals, because meiosis is completed only at fertilisation. As far as at least some genes are expressed and under selection during the male haploid phase, this would tend to bias towards tighter linkage in males. Sets of genes responsible for male-specific meiotic drive systems would be good candidates and are often found in tight linkage. Measuring the opportunity for haploid selection in animals may be possible within some groups. Imprinting may, however, act as a confounding effect in many groups of animals while trying to measure the opportunity for “haploid” selection. Within-species comparisons of imprinted regions or of regions with sex-specific recombination using high-resolution maps [20] may be more fruitful to discriminate among potential causes of heterochiasmy in animals. In particular, there is evidence in humans that the reduction in crossing-over associated with imprinting is in the direction that theory predicts, even if this pattern is consistent with other explanations [21]. Finally, understanding exceptions within groups (e.g., male marsupials, contrarily to most mammals, recombine more than females of the species [22]) may also shed light on the different hypotheses.

Heterochiasmy in Plants
We found that plant heterochiasmy is correlated with the opportunity for male and female haploid selection. Female meiosis tends to exhibit lower recombination rates relative to male meiosis when selection is intense among female gametophytes (e.g., in Pinaceae) or mild among male gametophytes (e.g., in highly selfing species). This pattern is expected if heterochiasmy is determined by the relative magnitude of haploid selection in male and female individuals. Finding a pattern consistent with this general population genetic prediction is, of course, not firm evidence that male-female dimorphism in haploid selection is the evolutionary force generating heterochiasmy. Other correlates of selfing rates might have to be closely examined [23]. However, we consider this explanation the most parsimonious so far. Our finding provides, therefore, the first empirical evidence for a theory explaining male-female differences in the amount of recombination and contributes to our understanding of contradictory observations that have puzzled geneticists for almost a century. It also indicates that the amount of recombination may be shaped by indirect selection, and, therefore, corroborates theories based on selection and variation for the evolution of sexual reproduction.