Sex didn’t always involve males and females. I know it still isn’t always between males and females, but that’s not what I mean. I mean that there was a time when sex was happening, but there were no males and females. Sex existed before males and females, and many species are still doing it without them.

There are a lot of characteristics we associate with maleness and femaleness: differences in body size, coloration, behavior, weaponry, genitalia, etc., but none of these things define males and females. Rather, it is differences in gamete size: males produce small gametes, and females produce large ones. And not all species produce two different sizes of gametes. The ones that don’t are called isogamous (“equal gametes”). Species that do produce unequal gametes are called anisogamous (“unequal gametes”) and, if they produce motile sperm and immotile eggs, oogamous.

The most recent common ancestor of eukaryotes was probably facultatively sexual, meaning that it could reproduce both sexually and asexually, and isogamous. Anisogamy (and therefore males and females) have evolved many times from this ancestral state, but many eukaryotic lineages are still isogamous. A new review article by Jussi Lehtonen, Hanna Kokko, and Geoff Parker reviews the origins of the sexes and proposes some ideas about how and why sex and the sexes may have evolved.

The article is in Philosophical Transactions of the Royal Society B: Biological Sciences, the oldest scientific journal in the world (well, one of the two, since it split into A and B in 1887). It’s also the journal in which Van Leeuwenhoek first reported the existence of Volvox (see “…of the bignefs of a great corn of fand” and “Best rejection letter ever, or science urban legend?“). Lest you think Philosophical Transactions sounds a bit stuffy, the issue in which the Lehtonen et al. paper appears is called “Weird sex: the underappreciated diversity of sexual reproduction.”

Although there are exceptions, there is a clear association between anisogamy and multicellularity: most multicellular organisms are anisogamous (or oogamous), and most unicells with described sexual cycles are isogamous:

There is a clear taxonomic link between isogamy and unicellularity. Although anisogamy does occur in unicells (e.g. in some species of the unicellular green algae genera Chlamydomonas, Carteria and Chlorogonium [6]), it is less common than isogamy. In multicells the reverse applies: while isogamy does occur, most multicellular taxa—including all metazoans and angiosperms—show anisogamy.

(Their reference 6 is Bell 1978) Interestingly, both kinds of exceptions occur in the Volvocales: not only anisogamous unicells but isogamous multicells as well:

…the multicellular colonial green algae genera Pandorina, Volvulina and Yamagishiella are isogamous

But these exceptions actually strengthen the association between multicellularity and anisogamy. The isogamous species within the volvocine algae rarely exceed 32 cells and lack a germ-soma division of labor. Larger species with cellular differentiation, such as Volvox and Pleodorina, are anisogamous, and these traits have probably evolved together at least twice within the volvocine algae. So the isogamous multicells in this group are barely multicellular (in fact, some authors don’t consider them truly multicellular), and when large body size and cellular differentiation evolved, anisogamy evolved along with it.

Turning their attention to the questions of how and why anisogamy evolves, the authors consider three scenarios in which anisogamy might evolve in different kinds of isogamous ancestors:

Group A—ancestral species with facultative sexual reproduction, which can be assumed to be capable of efficient asexual reproduction;

Group B—recently derived species with obligate sexual reproduction, with no constraints on the re-invasion of asexual reproduction, or constraints that are relatively easy to overcome;

Group C—species with long established obligate sexual reproduction with strong constraints that make the re-invasion of asexual reproduction extremely unlikely.

Just to clarify, facultative sexual reproduction refers to organisms that can reproduce sexually or asexually. This is true for a most single-celled eukaryotes and a lot of multicellular ones, including the volvocine algae. Obligate sex refers to organisms that only reproduce sexually. for example most vertebrates. If we assume that the most recent ancestor of eukaryotes was facultatively sexual, which is probably true, obligate sex can be seen as the loss of the ability to reproduce asexually. Sometimes, as in whiptail lizards, the ability to reproduce asexually is regained, but this is probably rare.

How does anisogamy evolve in each of these groups, given that males are key to the so-called twofold cost of sex? Since sperm make a negligible contribution to the size of the zygote, females must produce a gamete that is, all else equal, nearly twice the size it would need to be in an isogamous species. Note that this isn’t how the twofold cost of sex is usually framed; rather it is that a sexual population has the potential to reproduce twice as fast an an asexual one. But I want to emphasize that this cost is related to anisogamy.

The evolution of anisogamy has different effects depending upon which of the three groups it occurs in:

Group A is a priori capable of efficient asexual reproduction, making it easy to respond to an increasing cost of sex by engaging in the sexual cycle less often. Species in group B can relatively easily regain the lost capacity for asexual reproduction under increasing costs of sex. If a reversal to asexual reproduction appears, it has a high probability of invading in these two cases as the cost of males can be near twofold. As we have seen, anisogamy itself is unlikely to reverse. Groups A and B are, therefore, selected to re-evolve obligate asexuality: males and the capacity for sex are purged as sex becomes very costly. Group C is the only one in which anisogamy can invade such that sexuality remains unaffected. This group has adapted to and become reliant on sex to such an extent that asexual reproduction is unlikely to invade successfully. This makes the rising cost of males irrelevant: it can increase to twofold (or beyond) and sex can still be maintained. [references removed]

So the increasing cost of sex that accompanies anisogamy can cause the loss of sexual reproduction altogether in Groups A and B, but Group C is stuck with it. The authors conclude from this that most anisogamous groups probably evolved from ancestors in Group C:

The derived state…suggests a specific evolutionary pattern. Groups A and B are rare once they have reverted to asexuality, based on inferior evolutionary success over long timescales. Group C is the only one that avoids these adverse long-term effects after gamete sizes diverge: in spite of short-term costs of sex, the long-term benefits have ample time to operate because constraints prevent these lineages from reverting to asexuality. After anisogamy has evolved, sexual selection can reinforce the constraints making a return to asexuality even more difficult. At the same time, sexual selection and conflict increases the potential for ecological diversification. Thus, a relatively small number of group C species passing through the ‘anisogamy gateway’ can suffice to form the ancestors of the diversity of anisogamous life we see today. [references removed]

What about the cases in which anisogamy has clearly evolved from Group B ancestors? This they attribute to ecological differences between sexual and asexual forms:

…if ecological differences arise before the evolution of anisogamy, facultative sex may remain stable despite the evolution of anisogamy. This could explain the existence of groups of facultative sexuals with both isogamous and anisogamous species, such as volvocine algae.

One example of such ecological differences is the production of a resistant resting stage, a common outcome of sexual reproduction in facultatively sexual species (including volvocine algae).

The authors admit that their idea of an ‘anisogamy gateway’ as an explanation for the maintenance of anisogamous sex is speculative, but even so it

shows that there is a plausible pathway by which sex could have become an almost irreversible feature of multicellular life, even if it does not come with strong short-term benefits.

Their conclusion includes a line I rather like (but then I would, given what I study):

…even if our focus is on understanding multicellular organisms like ourselves, some of the most fruitful avenues to this may be found by also studying organisms that are very different from us.

 

Stable Links:

Bell, G. 1978. The evolution of anisogamy. J. Theor. Biol. 73:247–270.

Lehtonen, J., H. Kokko, and G. A. Parker. 2016. What do isogamous organisms teach us about sex and the two sexes? Philos. Trans. R. Soc. B Biol. Sci. 371:20150532.