From 11 Oct 2010.
I’ve been reading a few papers recently on the evolution of sex and it seems to me that an important distinction is often overlooked, the distinction between sex and gonochorism. Theoretical work on the evolution of sex often contrasts gonochoristic sexuality, i.e., having separate male and female individuals, with asexuality. If females have a constant number of offspring in gonochoristically sexual and asexual lineages, the asexual lineage will have twice the reproductive output. Suppose all females have four offspring; a gonochoristically sexual female will have two sons and two daughters, while an asexual female will have four daughters. Those four daughters will have four daughters, while the gonochoristically sexual female’s two daughters will each have two daughters. There are some simplifying assumptions here that may not hold–i.e., the sex ratio is 1:1, males are assumed to make only a genetic and not a material contribution to reproduction, and it is assumed that no physiological reliance on sexuality exists. The second is apparently the most problematic; if males provide food or other resources that can increase the per-female reproductive rate in a gonochoristically sexual species, a competing asexual female will not be able to achieve the theoretical doubling in reproductive rate. This is likely to be a factor to some extent among many mammals and birds, but presumably not in reptiles & insects. The third assumption has also been shown not to hold in some cases. Whiptail lizards (genus Aspidoscelis) have a hormonal reliance on mating behavior, and engage in pseudosexual behavior. This apparently reduces the efficiency of reproduction and prevents asexual whiptails from maintaining an equal per-female reproductive rate compared to their gonochoristically sexual relatives.
In any case, apart from the violations of simplifying assumptions that mitigate the potential doubling reproductive output of asexuals in some cases, the potential reproductive inequality between gonochoristically sexual and asexual lineages presents presents a significant challenge to any account of how sexuality could have evolved and how it could be maintained. Resolving this difficulty has been the focus of extensive research. However, as I suggested initially, I think the problem is in part poorly framed. The reproductive inequality that papers on the evolution of sex seek to address is not specifically one relating to sexuality vs. asexuality, but a result of the division of the sexes into separate individuals, i.e., gonochorism. If we compare hermaphroditic (loosely speaking… in plants this term and ‘gonochoristic’ can be misleading, see the post regarding Pollan’s “Botany of Desire” on PBS) lineages with asexual lineages there isn’t any general theoretical reason to expect a strong reproductive inequality between the two. All offspring in each case will be reproductive. We might expect marginally lower reproduction in hermaphrodites because some of their energy is devoted to male functionality, but, as the biological cliché goes, sperm are cheap; this should not be a major factor. We might still expect asexuality to be favored under certain circumstances, particularly if gamete (or, in flowering plants, pollen) transfer is inefficient. If populations are sparse and encountering other individuals of the species is infrequent or energy-intensive (or, in flowering plants, if pollinators are scarce or inefficient)–i.e., if it is difficult to engage in sexual activity–this should tend to favor asexuality. That aside, in general it seems to me that the arguments already advanced to explain the evolution of sex, which focus in various different ways on the fact that sex encourages genetic diversity, both in terms of numbers of alleles present and in their ability to be assorted in offspring independently of each other. Genetic diversity provides the substrate on which natural selection can act, and is thus a prerequisite for an evolutionary response to selective pressure. If either abiotic or biotic conditions change, a sexual species should be able to adapt to that change much more quickly and effectively.
Sexuality seems to me to be relatively easy to explain. Gonochorism, on the other hand, is very difficult to explain. Compare a gonochoristic and a hermaphroditic lineage; the latter should have twice (more or less) the reproductive output, but both have the genetic advantages of sexuality. The hermaphrodites should win easily. So, why are there so many gonochoristic species? I’m sure there must be literature that addresses this specific point, although I haven’t run across any in my own fairly cursory reading in the field, but I think many miss this point and simply take gonochoristic sexuality and asexuality to be the two available options. They are not.
(Parenthetically, a further confusion that I’m ignoring for present purposes is that between self-fertilization (or self-pollination…) and outcrossing. Self-fertilization is sexual, but has broadly similar detrimental genetic consequences to those asexuality. In plants, the evolutionary dynamics of self-compatibility / self-pollination vs. self-incompatibility are subject to some of the same general considerations as the evolution of asexuality vs. sexuality (which in plants is generally ‘hermaphroditic’, but occasionally ‘gonochoristic’…), but of course it isn’t quite the same. The main complication added is that selfing plants can be either facultatively or obligately selfing… anyways, enough for one day.)