Apparent independent and multiple evolution of binary sex

My friend Phil Ward at UC Davis found this reference and called it to my attention. It’s from the Philosophical Transactions of the Royal Society (B), and access is free (click on title below).  The pdf with the numbered references is here.

The paper is about how the evolution of two different types of gametes (“anisogamy”: a requirement for the origin of biological sexes) can originate from isogamy (same-sized gametes) under certain conditions. It is a theoretical paper, and I haven’t read it closely as I’m math-averse. However, what’s of interest is the first paragraph of the paper, which reviews the literature on anisogamy.  That paragraph states that anisogamy (ergo biological sex) has originated independently in many groups of eukaryotes (organisms with true cells).  I’ve put that first paragraph below and have bolded the relevant part. I’ve also linked to each group so you can see what they are.  The numbers lead to the references, which I have not checked.

Multicellular organisms typically produce gametes of two distinct size classes: larger eggs and smaller sperm. This dimorphism—known as ‘anisogamy’—is a remarkable case of convergent evolution. It has arisen independently in multiple distantly related eukaryotic lineages, including in animals [1]; dikaryotic fungi [2]; various groups of green algae, including the ancestors of land plants [3,4]; red algae [5]; brown algae [6,7]; yellow-green algae (Xanthophyceae: Vaucheria) [8]; diatoms [9]; oomycetes [10]; dinoflagellates [11]; apicomplexans [12]; and parabasalids (Trichonympha) [13]. By contrast, the gametes of most unicellular and some multicellular eukaryotes are isogamous, with a unimodal distribution of gamete sizes. Anisogamy is often taken as the defining difference between ‘male’ and ‘female’ sexual strategies: males produce only sperm; females produce only eggs; and hermaphrodites have the potential to produce both gamete types, either simultaneously or at different life stages. Isogamous species lack sexes by this definition. However, their gametes can often be classified into two, or occasionally more, ‘mating types’, such that fertilization only occurs between gametes of unlike types [2,14–16].

If you add up these groups, you get at least 11 evolutionarily independent origins of anisogamy: the production of “larger eggs and smaller sperm.”  The independence is probably inferred via a “cladistic” method by looking at the family trees of these groups, seeing that the ancestors were either asexual or isogamous, and noting that anisogamy appeared on a later-appearing derived branch.

If the authors are indeed correct, then what we have here is a remarkable example of evolutionary convergence: eleven separate groups independently evolving binary sex with large eggs and small sperm.  There are of course evolutionary theories showing why an ancestral condition of sex with equal-size gametes would split into a derived condition with two sizes of gametes, but that is a theoretical result.  Here we see that this has actually happened in nature nearly a dozen times, so the theories may hold some water.

I’ll add one thing. Not only has anisogamous sex apparently evolved eleven times independently, but, even in the one group of animals the determinants of sex—the features that trigger the development of two types of animals producing different-sized gametes—have also evolved independently. Luana and I pointed this out in our paper, “The ideological subversion of biology” (bolding is mine):

We can see the stability of the two-sex condition by realizing that what triggers the development of males versus females varies widely across species (Bachtrog et al. 2014). Different sexes can be based on different chromosomes and their genes (e.g., XX vs. XY in humans, ZW vs. ZZ in birds, individuals with like chromosomes being female in mammals and male in birds); different rearing temperatures (crocodiles and turtles); whether you have a full or half set of chromosomes (bees); whether you encounter a female (marine worms); and a host of other social, genetic, and environmental factors. Natural selection has independently produced diverse pathways to generate the sexes, but at the end there are just two destinations: males and females. And so we have an evolved and objectively recognized dichotomy—not an arbitrary spectrum of sexes.

Now I’m not smart or diligent enough to figure out why once there are two sexes—which is the case in animals, and must thus have been true in our common ancestor)—how you can evolutionarily traverse from one determinant of sex (say a gene on a chromosome) to something like temperature-dependent sex determination or social sex determination (e.g. the famous clownfish, used by miscreants to claim that there are more than two sexes).  It’s a mystery waiting to be solved.  But so even here, in one group, we have convergent evolution—of the factors that cause the two sexes to diverge.

I find all this fascinating, and it shows the power of Orgel’s Second Rule: “evolution is cleverer than you are.”