Sexual reproduction: a poorly understood and recurrent evolutionary dilemma
Already for Darwin (1871), sexual reproduction and sexual selection appeared as a specific, but difficult problem. Since these times much attention has been paid by both evolutionists and developmental biologists to the understanding of sexuality, but a deep gap still persists between the two approaches.
In most animal species sexes are separated, about 50% of individuals are males, 50% are females. From an ecological and evolutionary point of view, this proportion is not an optimum. Optimising selection should favour species in which there are more females than males. Why this is not so is generally explained by genetical constraints. In most species, sex appears to be transmitted as a simple Mendelian character, leading to a 50-50 segregation. Only in a few groups, such as reptiles or haplodiploid arthropods, sex is not genetically determined, and the sex ratio may vary, often in an adaptive way, i.e. producing more females than males.
Indeed, the occurrence of sexual reproduction is, within evolutionary theory, a puzzle and a dilemma. It is commonly argued that sexual reproduction which implies not only fertilisation, zygote production and embryonic development, but also genetic exchanges among different individuals of the same species, is a means for conserving the genetic diversity, keeping the genetic load at an acceptable level and permitting eventually new adaptations and evolutions.
But all these are supposed long-term advantages, in opposition with short-term disadvantages (Maynard Smith 1978). Although most animals are gonochoric (two sexes) many are parthenogenetic, that is reproduction occurs without fertilisation and by a direct development from female gametes. Parthenogenesis is a recurrent phenomenon which has evolved independently from bisexual species in many groups. From a theoretical point of view, it is easy to show that a parthenogenetic mutant, appearing in a bisexual species, should invade the population and outcompete the gonochoric form. In other words, parthenogenesis should be the general way of reproduction, and why it is not so remains a dilemma. Evolutionists are obliged to suggest ad hoc arguments, and the most general one is that parthenogenetic organisms are made of clones with a low genetic diversity. This should prevent their adaptation to changing environments and result in high rates of extinction. In other words, the short-term advantage of parthenogenesis should be counterbalanced by a long-term disadvantage. It is also possible, for example in Mammals, that parthenogenesis is not possible due to genetic imprinting and the differential expression of genes coming from the sperm or the oocyte in the embryo.
Developmental biologists have also long been fascinated by sexuality. In Vertebrates, we know than sex hormones play a major role in the differentiation of primary and secondary sexual characters. In Drosophila, on the other hand, each cell is autonomous and capable of expressing independently its own sexual genotype and no hormones are involved.
Sex differentiation has been analysed not only by classical experiments of developmental biology such as grafts and extirpations, but also by genetic means. Indeed, it has been the first great success of developmental genetics. To summarise the results shortly, sex is determined in Drosophila by a succession of genetic cascades acting within each cell. In Mammals, the primary induction of the male hormone in the testis will eventually determine the whole male phenotype. In the female, the absence of male hormone permits the differentiation of the female phenotype.
Sexes are phenotypes which are very strongly constrained, or canalised, by natural selection. Individuals must be normal males or normal females for mating and reproduction. Genetic dissections of sexual phenotypes have produced intermediate individuals which are almost always abnormal and sterile. So the question is: 'How is the genetic determinism of sex able to evolve?'
The strong constraints existing on phenotypes suggest that, as for the antero-posterior axis of early embryos, we should find genetic homologies in sex determination of distantly related taxa. Developmental genetics did show exactly the reverse. The genetics of sex determination is a fast evolving trait; sexual phenotypes are pure analogies. Different evolutionary pathways are visible not only between distant taxa (e.g. arthropods and vertebrates) but also within arthropods (Bull 1983): for example, a sex hormone, the androgenic hormone is responsible of male differentiation in Crustacea. Even within the same insect order, major differences are found: genetic determinisms of sex in houseflies or mosquitoes are very different from that of Drosophila.
Here is a clash between developmental and evolutionary biology. Developmental genetics has revealed a high diversity among mechanisms of sex determination, presenting sex as a relatively fast evolving trait producing analogous phenotypes. Evolutionary biologists, however, cannot understand and explain how it is possible to evolve from one genetic system to another one, since any genetic change is likely to produce abnormal, sterile individuals. The only possibility I can see for the moment is that such a transition might occur by the intermediary of a relatively neutral form, that is, a parthenogenetic lineage. In such a lineage, stabilising selection on sexual phenotypes would be released, permitting some genetic changes. In the long-term, but for unknown reasons, a new male phenotype could appear with an original genetic basis. Of course, this hypothesis requires further theoretical analyses, in order to understand why and how a neo-male might occur.
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