Evolution of outcrossing and selfing

Sex is costly. You could die trying to find a mate. Your mate could kill you, or give you a disease. You could be unable to find a mate in the first place, in which case you’d be better off if you could reproduce asexually. Even without those risks, though, even in a simple genetic simulation, sexual reproduction means you only pass on half of your genes to your offspring.

So why do it? We know that it’s possible to reproduce without sex; lots of things do. It’s not just bacteria and protists, either: asexual reproduction occurs in some plants, insects, snails, amphibians, and reptiles, among many others. The logic of natural selection suggests that sex must confer some benefit that outweighs all the costs, at least in some situations. Essentially all of the proposed benefits of sex have to do with outcrossing, or mixing your genes with those of another, genetically distinct, individual.

Nevertheless, a lot of things that reproduce sexually do so without outcrossing. This is especially common in plants, where it’s called “self-pollination” or just “selfing.” Selfing is thought to provide short-term advantages relative to outcrossing–basically by avoiding the costs I’ve listed above. However, selfing also doesn’t provide most of the benefits associated with sex, so it’s thought to be a bad strategy in the long term. This leads to selfing being thought of as a “dead-end” strategy: the short-term advantages make it unlikely that a selfing species will return to outcrossing, and the reduced genetic variation produced by selfing make diversification less likely.

Erik Hanschen and colleagues have tested these predictions in the volvocine algae (I’m among the “colleagues,” as are John Wiens, Hisayoshi Nozaki, and Rick Michod): do selfing species ever return to outcrossing, and do they have a lower rate of diversification than outcrossing species? Both mating systems exist within the volvocine algae, and so they make a good test case. Roughly speaking, the term heterothallic refers to outcrossing species and homothallic to selfing species:

Hanschen et al. Fig. 1

Figure 1 from Hanschen et al. 2017. Diversity of mating systems in the volvocine green algae and their respective life cycles. (A) In outcrossing (heterothallic) species, distinct genotypes (male on left and female on right) sexually differentiate producing either eggs or sperm. A diploid zygospore (red) is produced after fertilization. Sexual offspring hatch and enter the haploid, asexual phase of the life cycle. (B) In selfing (homothallic) monoecious species, a single genotype is capable of producing both gamete types. Upon sexual differentiation, each sexual colony produces both sperm and eggs. (C) In selfing (homothallic) dioecious species, a single genotype sexually differentiates, producing either eggs or sperm, but not both within the same colony. Cartoons in panels (A–C) are shown with anisogamous, Volvox-like morphology for illustrative purposes only.

But this is a case where being happy with ‘rough’ definitions can get us into trouble, especially since they’re used a bit differently in other groups. Heterothallism, at least in the volvocine algae, is basically synonymous with genetic sex (or mating type) determination. In other words, a given genotype of a heterothallic species can produce either sperm or eggs, never both. This leads to obligate outcrossing, because a spheroid can never mate with another of the same genotype.

In homothallic species, a given genotype can produce both sperm and eggs, so it is possible for two spheroids of identical genotype to mate. This situation comes in two flavors, monoecious and dioecious (B & C, respectively, in the figure above). Sexual spheroids of monoecious species are hermaphrodites: a single spheroid produces both sperm and eggs. In dioecious species, a single genotype will produce separate male and female sexual spheroids, the males producing sperm and the females producing eggs. A third flavor of monoecy, not represented in the figure, is androdioecy, in which a single genotype produces both hermaphrodite and male spheroids (for more on this, see “Another step toward understanding sex determination in Volvox“).

So heterothallic species are obligate outcrossers, i.e. sexual reproduction always involves two genotypes, and homothallic species are facultative selfers, i.e. sexual reproduction can involve one genotype (selfing) or two (outcrossing). Does outcrossing ever evolve from selfing? This is predicted to be rare, because the short-term benefits of selfing prevent invasion by an outcrossing genotype. Hanschen and colleagues used ancestral character state reconstructions to test this:

Hanschen et al. Fig. 2

Figure 2 from Hanschen et al. 2017. The evolution of outcrossing (black) and selfing (green). Branch color refers to the most likely state inferred by maximum likelihood (ML) reconstruction. Pie charts at nodes represent scaled marginal likelihoods from ML reconstruction. Numbers at select nodes indicate Bayes factors (support for that character state against the next most likely state), which explicitly take phylogenetic uncertainty into account, colored by which state is most supported. Interpretation of Bayes factors (Kass and Raftery 1995): 0–2 barely worth mentioning, 2–6 positive, 6–10 strong, >10 very strong. Chlamy., Chlamydomonas; Astre., Astrephomene; Col., Colemanosphaera; N., NIES; U., UTEX.

Let’s zoom in on one particularly interesting part of that reconstruction. Here’s the group known as “section Volvox” (or sometimes Euvolvox) and its closest relatives:

Section Volvox

Within section Volvox, only two species are heterothallic: Volvox perglobator and Volvox rousseletii. Thus it seems likely that the most recent common ancestor of this group was also heterothallic. In this case, Volvox perglobator and Volvox rousseletii must have evolved homothallism, in other words lost genetic sex determination. If, on the other hand, the most recent common ancestor of section Volvox were homothallic, this would imply that several lineages evolved genetic sex determination (heterothallism) independently:

Alternative reconstruction

In the first reconstruction, three changes are required: from heterothallism to homothallism near the base of the section Volvox part of the tree, then two changes from homothallism to heterothallism in Volvox perglobator and Volvox rousseletii. In the second, four changes are required, all from the ancestral heterothallic state to homothallism: in Volvox kirkiorum, in Volvox ferrisii, in Volvox barberi, and in the most recent common ancestor of Volvox globator and Volvox capensis.

In this kind of reconstruction, the path that requires the fewest changes is preferred. This is called the most parsimonious reconstruction. It’s preferred because species inherit most of their traits from their ancestors. Some things change; most remain the same (a concept I attempted to explain to Cornelius Hunter). Humans, for example, inherited most of our traits from our common ancestor with chimpanzees. Yes, we are bipedal and have less hair and bigger brains, among many other derived traits. But we have many more traits that are inherited: forward-facing eyes, absence of a tail, nails instead of claws, five digits, seven cervical vertebrae, placenta, mammary glands, endothermy, mitochondria, and on and on. All the traits we share with other apes, primates, mammals, vertebrates, animals, and eukaryotes. Change is the exception rather than the rule, so all else equal a reconstruction that requires fewer changes is more likely to be true (Hanschen et al. actually used likelihood and Bayesian methods rather than parsimony, but the basic principle of ‘fewer changes are better’ remains the same).

So at least in this case, the most parsimonious reconstruction has two outcrossing species, Volvox perglobator and Volvox rousseletii, descending from selfing (homothallic) ancestors. If that’s right, it means that the idea that the short-term benefits of selfing prevent invasion by an outcrossing genotype is wrong, or at least not always right. Furthermore, selfing does not seem to prevent speciation; along with section Volvox, the clade that includes Pleodorina californicaPleodorina japonica, and Volvox aureus seem to have diversified from a selfing ancestor.

The long-term persistence of selfing in volvocine algae may be due, at least in part, to their life cycle. Volvocine algae are ‘haploid dominant’, that is, the multicellular phase of their life cycle has only one set of chromosomes. Most of the multicellular organisms we’re used to thinking about are diploid dominant, i.e. they have two sets of chromosomes in the multicellular stage. This is true for animals, for example, where the haploid stage of the life cycle is unicellular and ephemeral: the gametes. In diploid-dominant organisms, selfing can lead to inbreeding depression, a reduction in fitness due to increased homozygosity. A lot of detrimental traits are only expressed when both gene copies are the same, and inbreeding makes this more likely. Self-fertilization is the most extreme version of inbreeding; just one generation of self-fertilization means that every gene is homozygous in the offspring. Since homozygosity is not an issue for haploid organisms, it may be that the costs of selfing are lower than in diploids.

There’s another possible reason that the balance of costs and benefits of selfing may be different in volvocine algae, one that we didn’t mention in the paper. We classified homothallic species as selfing, but they are really only facultatively selfing; they are perfectly capable of outcrossing if genetically distinct individuals are around when they start mating. In a genetically diverse population, only a tiny minority of matings will be between genetically identical individuals. In this case, the costs of selfing may be low simply because it doesn’t happen that much.

When selfing is likely to happen is when diversity is low. This could well be the case in some situations, for example when a single individual has dispersed to a new pond. Such an individual would likely reproduce asexually for a while, and its progeny would eventually enter the sexual phase. If no other individuals had shown up by then, all of the matings would be between genetically identical (or nearly so) individuals. Nevertheless, a homothallic individual that colonizes a new pond is probably better off than a heterothallic one. When volvocine algae have sex, usually in late summer or fall, they produce a dormant spore that is resistant to cold, desiccation, and other environmental insults (red circles in Figure 1 above). The progeny of a heterothallic colonist would be unable to mate, unable to produce spores, and therefore unlikely to survive the winter.

So the life cycle and ecology of volvocine algae might lead to different costs and benefits of selfing than we’re used to thinking about. A haploid dominant life cycle means that inbreeding is much less of a problem, and the ecological utility of sexually-produced spores might make a homothallic colonist more likely to survive the first year in a new environment than a heterothallic one. Facultative homothallism might provide volvocine algae with the benefits of outcrossing (when other genotypes are around) without the cost of potentially being unable to find a mate. From this perspective, we might want to ask not why homothallism persists in volvocine algae, but rather why it is so rare!


Stable links:

Hanschen ER, Herron MD, Wiens JJ, Nozaki H, and Michod RE. 2017 Repeated evolution and reversibility of self-fertilization in the volvocine green algae. Evolution (doi: 10.1111/evo.13394)

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