Continued hope for a general explanation of sex

Some natural phenomena may defy explanations in terms of single causes. The genetic basis for Haldane's Rule, for example, depends in part on whether the rule manifests itself in terms of hybrid inviability or sterility and varies among taxa (Orr, 1997). West et al. (1999) suggest that the widespread occurrence of sexual reproduction similarly requires multiple explanations. Currently, neither models of mutation accumulation nor those of changing environments, notably the Red Queen, can on their own fully account for the maintenance of sexual reproduction given the two-fold advantage of asexuality. The motivation for West et al.'s argument makes sense: creatures typically suffer from parasites as well as from deleterious mutations, and sexual reproduction may be the best way to ®ght their combined attack. This may be especially true, they argue, because both processes can complement each other and act synergistically. Encouraged by successful simulations of a number of speci®c cases (e.g. Howard & Lively, 1998), the authors invite further work in this area. We agree with West et al. in that an integrated approach is required to explain why sex abounds. After decades of thorough exploration, all potentially contributing factors have probably been identi®ed. The discovery of yet another mechanism that could instantly solve the riddle seems doubtful. However, we are sceptical that the way forward lies in the analysis of pairwise or multiple interactions of potential causes as proposed by the authors. Imagine for the moment that speci®c interactions of deleterious mutation loads and parasite±host dynamics can account for the maintenance of sexual reproduction. The parameter space that covers these dynamics will not be easily de®ned but is extremely large. The list of factors that need to be speci®ed includes the rate of mutation and the distribution of mutational effects, the genetic basis of the parasite±host interaction, as well as the resulting multivariate ®tness functions. The Red Queen dynamics alone have been modelled in a variety of different ways (Otto & Michalakis, 1998), some or all of which may be fair representations of some natural systems. The crucial point is that any one of the resulting models is necessarily speci®c, and its analysis is complex. A thorough exploration of a general phenomenon via a collection of speci®c models seems a daunting task. If the widespread occurrence of sexual reproduction indeed required such a compartmentalized analysis, then we would be a long way from understanding the problem. This would quite simply be sad. However, the situation may not be quite so bleak. The need for a collection of distinct models would arise if the region of the parameter space in which sex is favoured had a complicated shape and was possibly even disjunct. We ®nd this hard to imagine. Why should the vast majority of taxa exist in exactly these speci®c pockets and branches of the parameter space and why should they restrict their movements to these regions as they diversify and speciate? It appears much more likely that the relevant region is large and continuous, in which case there should be a general explanation for the maintenance of sexual reproduction. This argument does not deny the usefulness of speci®c models to explain the recurring yet isolated emergence of asexual lineages. West et al. call for detailed case studies aimed at parameter estimation. We agree that such studies would be extremely useful in order to understand just what sets the balance of forces in favour of asexuality in these cases. While the yardstick of a two-fold advantage for asexuals is a useful shorthand, it does not apply universally even in anisogamous species. The bene®t of paternal care in some breeding systems is only one example. Depending on the genetic mechanisms that bring about the transition to parthenogenesis, the relative ®tness of asexuals may be either smaller or larger than two. For example, a new parthenogen that arises through the duplication of one haploid genome of its sexual parent would be entirely homozygous. Aside from the obvious case of recessive lethals, there should be a ®tness loss due to the large class of mutants that are slightly deleterious and partially recessive. The number of such mutations in the new parthenogen need not be large to melt away the two-fold advantage. A better understanding of the genetic mechanisms of asexuality seems therefore necessary. We believe that the explanations for particular cases of asexuality may well be varied. As a consequence, they differ from the reason why the vast majority of taxa reproduces sexually. We remain hopeful that an explanation for the maintenance of Correspondence: B. NuÈ rnberger, Zoologisches Institut der Ludwig-Maximilians-UniversitaÈt MuÈ nchen, Karlstr. 23±25, 80333 MuÈ nchen, Germany. E-mail: nurnbb@zi.biologie.uni-muenchen.de