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Background: To the best of my knowledge, most sexually-reproducing species of organism have two sexes, although there are also sexually-reproducing species of organism (flatworms come to mind) which have only one sex. (Depending on one's definition of sex.)

Many species of fungi are both sexually reproducing and apparently have more than two sexes. (Depending on one's definition of sex.)

There are also species of lizards with more than two biologically determined "gender morphs". It is even more debatable than in the case of fungi whether these morphs should be considered separate "sexes" or not, since their mating compatibility network is bipartite.

Question:
Is there a theoretical maximum on the number of sexes a given species of organism can have?

Elaboration: There would also be a lot of different possibilities -- already with three sexes, one can imagine at least two different means by which sexual reproduction could occur -- any one of three combinations of two individuals from two distinct sexes (most likely in "rock-paper-scissors" fashion), or the combination of three individuals from all three distinct sexes.

How, for example, might either of these two scenarios be maladaptive compared to sexual reproduction of two individuals in species with two or fewer sexes?

I am asking about species with more than two sexes/mating types in general, not necessarily about situations where more than two sexes are involved in a single reproductive event. (Contrast with this related question.) I am also not restricting to animals, or even multi-cellular organisms, or even eukaryotes, since these restrictions might affect the answer. (Contrast with this related question.)

Note that this answer to the second related question implies that we should expect the mating compatibility network of anisogamous sexually reproducing organisms to be bipartite. But note that, as in the example of the side-blotched lizards, this doesn't necessarily preclude having more than two sexes, nor does it give a theoretical maximum to the number of possible sexes. And since I don't want to necessarily restrict to anisogamous sexually reproducing organisms (i.e. isogamous ones would also be fine), then that answer also does not provide a theoretical maximum for isogamous sexually reproducing organisms either.

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    $\begingroup$ I just upvoted it, now it's back to zero (and OP got 8 points). Too bad this was closed: I have an answer explaining that there is no limit to the number of sexes when there is no syngamy and therefore cytoplasmic inheritance, like in protozoa conjugation. Actually, there is no mention to animals in the question's title, it just say organisms. $\endgroup$
    – user24284
    May 18 '17 at 3:22
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    $\begingroup$ By the way, flatworms have two sexes, which happen to be (in some classes but not all) in the same individual. $\endgroup$
    – user24284
    May 18 '17 at 6:50
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    $\begingroup$ @Chill2Macht That being the case, I suggest you edit your question, making it clearly that the question is about organisms in general (as the title is), not only animals, so we can cast reopen votes. Also, you may want to clarify if you're talking about organisms or species. Thus, I'd do something like "Is there a theoretical maximum on the number of sexes a given species can have?" $\endgroup$
    – user24284
    May 18 '17 at 7:42
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    $\begingroup$ So, we have a problem here: do you want to know if a given species can have more than 2 sexes, or if a given organism can express more than two sexes (be it at the same time or not)? They are tottaly different questions. The species in my (future) answer, for instance, have 8 sexes, but each individual has only 1 sex. $\endgroup$
    – user24284
    May 18 '17 at 8:17
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    $\begingroup$ Ok, I just casted a reopen vote. However, I believe the best idea is just forgetting about this question and posting a new, fresh one. $\endgroup$
    – user24284
    May 18 '17 at 9:17
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Well, your question as a whole is quite broad, with a lot of sub-questions or items (and some inaccuracies, as in the case of flatworms) . That being said, in this answer I'll address only your main question (and nothing more), which is ipsis litteris:

Is there a theoretical maximum on the number of sexes a given species of organism can have?

All the content in this answer is based on this excellent book from Michael Majerus, Sex Wars: Genes, Bacteria, and Biased Sex Ratios:

enter image description here

Unfortunately, I don't have my library anymore and I can't find this book online. So, instead of (boringly) quoting the author, I'll try to summarise his hypothesis. Of course, to a better explanation, you can read the book itself.

Let's start supposing that you're pretty comfortable with the concept of sexual reproduction and sexual types, which I think you are.

Suppose we have two sexual types, called A and B. They have receptors in their gametes' membranes, in such a way that you cannot fusion A + A or B + B gametes, but you can fusion A + B gametes. If the A gamete could fertilize another A gamete, you'll have all gametes in a given gonad fertilising each other, which makes no sense. So, will assume that a given sexual type has mechanisms to avoid fertilising the same sexual type.

So far, what I described is the common system with two sexes, be them "+ and -" or "male and female", it doesn't matter.

Now, let's suppose three sexual types: A, B and C. For this to work, their membrane receptors must be such that A can recognise B and C, but not A. This is theoretically possible (although it is a mess genetically speaking). Thus, the possible matings are:

  • Sexual type A → A + B and A + C;
  • Sexual type B → B + C and B + A;
  • Sexual type C → C + A and C + B;

A system with 3 or more sexes has obvious advantages. Right now, for instance, in a population with two sexual types and the same sex ratio, one has 50% (1/2) of the individuals in that population as potential mate. But, supposing a sex system with 5 sex types (A, B, C, D and E), any individual would have 80% (4/5) of the individuals in that population as potential mate.

So, why cannot we find sexual systems with more than two sex types?

The answer is: we can, but not among species which perform fertilization (animals, plants, most of fungi, most of algae etc...).

This is the problem: in fertilization, or syngamy, the gametes don't simply join their nuclei. It's more complex than that: there is cytoplasmic inheritance, or extranuclear inheritance.

To keep the example among animals, the group you said you know best: mitochondria in the zygote comes from only one gamete (the female one). That happens to avoid what we call heteroplasmy, which is the presence of more than one type of organellar (mitochondrial, in this case) genome in the zygote.

In sex systems with only two sexual types the rule is very clear: "mitochondria comes from this one, but not from that one". That's it, case solved.

But what happens with our system with three (A, B and C) sexual types? If you define that when A mates with B only A donates the mitochondria and, similarly, if you define that when A mates with C only A donates the mitochondria, who donates the mitochondria when C mates with B? Do you see? There is no possible rule here!

Therefore, cytoplasmic inheritance is, probably, what avoids the evolution of more than 2 sexual types.

How can we support this claim?

Let's find what happens in species that perform sexual reproduction, but no fertilization (and, therefore, don't have the cytoplasmic inheritance problem). The best example are protozoans that perform conjugation.

Tetrahymena is a well known example. In these protozoans, according to Umen, 2013:

An individual Tetrahymena cell expresses one of seven possible mating types (I–VII) that it faithfully and indefinitely maintains during vegetative propagation. After mating each new exconjugant has a recombinant micronucleus formed from its two parents. However, rather than just expressing one of two parental mating types, the sexual progeny of Tetrahymena undergo a kind of genetic roulette that allows them to choose at random up to seven possible mating types. (emphasis mine)

So, we have sex mating types. How that system works? According to Cervantes et al., 2015:

The unicellular eukaryote Tetrahymena thermophila has seven mating types. Cells can mate only when they recognize cells of a different mating type as non-self.

Thus, if you belong to sexual type I you can mate with someone that belongs to sexual types II, III, IV, V, VI or VII. The same way, if you belong to sexual type II, you can mate with someone that belongs to sexual types I, III, IV, V, VI or VII, and so on...

The record, however, probably belongs to the basidiomycete Schizophyllum commune, with more than 28.000 sexual types! (Whitfield, 2004) To support the idea that cytoplasmic inheritance is in fact the main factor that avoids more than 2 sexual types, it's worth noting that biparental mitochondrial transmission is quite common in fungi (Barr, Neiman and Taylor, 2005).

Sources:

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  • $\begingroup$ This is a great answer, thank you! However, I should note that, since species with two sexes evolved from hermaphroditic ancestors (e.g. sciencedaily.com/releases/2008/11/081120171328.htm), it makes more sense to say that hermaphroditic species have only one sex, rather than each individual displaying two sexes (which is a very anthropocentric point of view). Also, the claim that species undergoing fertilization don't display more than two sexes is also untrue. For example, isogamous fungi are known to have more than two mating types. $\endgroup$
    – Chill2Macht
    May 20 '17 at 6:00
  • $\begingroup$ blog.mycology.cornell.edu/2010/06/02/… Isogamous organisms do undergo sexual reproduction via fertilization rather than conjugation: yourarticlelibrary.com/reproduction/… The side-blotched lizards are anisogamous, yet have more than two gender morphs (but a bipartite mating compatibility network). That being said, the argument presented is accurate if we restrict to anisogamous organisms (and recognize the possibility of bipartite networks with more than two nodes). $\endgroup$
    – Chill2Macht
    May 20 '17 at 6:08
  • $\begingroup$ For example, Schizophyllum commune, which is mentioned in the answer, does undergo fertilization, but it is isogamous. journals.plos.org/plosbiology/article?id=10.1371/… It is not a protozoan, and it does not undergo conjugation. It therefore has to deal with cytoplasmic inheritance. Therefore, the underlying premise of the answer (that cytoplasmic inheritance prevents the development of more than two sexes in all species undergoing fertilization/syngamy) appears to be generally incorrect, and partially correct only for anisogamous organisms. $\endgroup$
    – Chill2Macht
    May 20 '17 at 6:14
  • $\begingroup$ This webpage better confirms the fact that Schizophyllum commune undergoes plasmogamy botit.botany.wisc.edu/toms_fungi/feb2000.html i.e. joining of cytoplasm during mating. So the information described in the paper journals.plos.org/plosbiology/article?id=10.1371/… regarding the problem of number of sexes and cytoplasmic inheritance seems unfortunately incomplete, since it seems to fail to adequately explain or address isogamous fungi. Note also that it mentions that Hamilton and Hurst were unable to confirm their hypothesis. $\endgroup$
    – Chill2Macht
    May 20 '17 at 6:25
  • $\begingroup$ In the paper you linked to journals.plos.org/plosbiology/article?id=10.1371/… , Professor Michiels (at the very end) also states that he believes that two-sexed animals evolved from hermaphroditic organisms, again supporting the claims that hermaphroditic species should be considered as having one sex. That being said, as the paper makes very clear, the definition of the word "sex" is actually very muddied, such that the number of sexes which a given species has depends entirely on one's choice of definition, which is a matter of opinion, not of fact. $\endgroup$
    – Chill2Macht
    May 20 '17 at 6:35

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