by Piter Kehoma Boll
During the evolution of life, sex was certainly a great innovation. It allows organisms to reproduce while mixing their genes with that of another individual. Although it usually makes your offspring to have only half of your genes, which does not seem to be as great as an offspring that carries you as a whole into the next generation, there are certainly advantages in mixing. The most evident advantage is that your genes can combine with other versions and, as a result, produce a better team of genes than the one that you had. Even though each of your children carries only half of you, that half is more likely to survive than a child that carries you as a whole. In other words, sex gives the possibility for a population of genes (those that make up an individual) to get rid of some of the less efficient ones and replace them with better copies.
As you know, most sexual organisms make such a recombination by fusing two sexual cells, the gametes, and those are usually of two different kinds: a small one (the male) and a large one (the female).
In some species, each individual can only produce either male or female gametes, therefore being either a male organism or a female organism. In such species, sexual reproduction requires a male to mate with a female. This is the pattern found, for example, in most vertebrates and arthropods.
A female (large) and a male (small) of the tick Ixodes ricinus mating. Image by Jana Bulantová.*
In other species, each individual can produce both male and female gametes, therefore being called a hermaphrodite. The advantage of such a system is that hermaphrodites can mate with any individual of their species, sometimes even with themselves! One of the main problems with hermaphroditism is when you decide to play only one role, which may lead to conflict during sex.
Two snails Helix pomatia (hermaphrodites) making love. Photo by Wikimedia user Jangle1969.**
Now what evolved first? Dioecious species (those having male and female individuals) or hermaphrodites (allso called monoecious species)? It’s hard to tell, but we can be sure that during evolution many lineages switched from one system to the other and back. And the coolest part is that such switches still happen today.
You may know that most flowering plants are hermaphrodites. Flowers usually have both male and female organs, although they are rarely able to fertilize themselves (self-fertilization). Among plants, the cases of dioecious species seem to be mainly due to some mutation that ended up partially sterilizing an individual. For example, a mutation could appear that makes the plant unable to produce male organs, thus becoming only female. Other individuals in the population that lack this mutation continue to be hermaphrodites, so we have an “unbalanced” species with two sexes, females and hermaphrodites, but no males. Although unusual at first, such a system can remain stable if reproduction occurs through cross-fertilization and not self-fertilization. As both females and hermaphrodites need pollen (which produces the male gametes) from other plants, they can coexist as long as the pollinator carries pollen to both sexes. The same happens if the sexes are male and hermaphrodite. As long as the pollinator carries the male’s pollen to hermaphrodite flowers, both sexes can do just fine.
The plant Geranium sylvaticum includes hermaphrodites and females, but no males. Photo by Enrico Blasutto.**
Species composed of males and hermaphrodites are called androdioecious (from Greek andro-, man, male + di-, two + oikos, home, house; therefore “male in two “houses”, i.e., in two different kinds of organisms), while those composed of females and hermaphrodites are called gynodioecious (from Greek gyno-, woman, female; therefore “female in two different kinds of organisms).
Androdioecious and gynodioecious species occur among animals as well, but in this case their existance indicates something happening in the other direction, i.e., it is a transition from a dioecious species (with males and females) to a hermaphrodite species. And this is much more complicated that the other way round. Actually, it can get really, really bad for the “single-sex sex”.
This unbalanced sexual system in animals usually happens like this. There is a happily dioecious species with male and female individuals, but one day a new mutation appears and allows one of the sexes to produce both male and female gametes, thus becoming an hermaphrodite. However, such hermaphrodites are usually unable to play the role of the new sex while mating, i.e., they have the gametes, but not the tool to mate using them. Thus, the only way to use both gametes is to fertilize themselves.
One problem that comes from doing that is inbreeding. When you fertilize yourself, you are not increasing genetic diversity. On the contrary, you have very high chances of producing offspring with two copies to the same gene, thus decreasing genetic diversity. In order to continue to have recombination, you must mate with the single-sex individuals, which means you can only play the role of your original sex and your hermaphroditism is irrelevant. You are producing useless gametes. Or are you?
A male and a hermaphrodite of the nematode Caenorhabditis elegans an androdioecious species. Credit to Worm Atlas.
The problem with inbreeding happens when an organism ends up with two copies of a deleterious gene, which is fairly common in species where cross-fertilization is the rule and such deleterious genes are maintained in the population through individuals with a single copy that is not enough to cause any trouble. That is why having kids with your parents, children of siblings is usually a bad idea. When a species evolves from a system of cross-fertilization to one of self-fertilization, inbreeding can be a serious problem at first, producing many descendants that will die soon. However, eventually this will “purge” the set of genes. If individuals only mate with themselves, the number of deleterious genes will sharply decrease after some generations and inbreeding will not be such a big problem anymore.
When this happens in a species with unbalanced sex, the single-sex individuals will be in trouble. Two androdioecious animals have been studied regarding this conflict, the nematode and model organism Caenorhabditis elegans and clam shrimps of the genus Eulimnadia, such as Eulimnadia texana. In both groups, the hermaphrodites do not seem to be very interested in mating with males. They have even lost most phenotypic clues that help males identify them as potential mates. The only thing left for the males is to insist, to look for hermaphrodites and force them to mate with them, but it is a hard battle. Even when mating does occur, the hermaphrodite usually discards the male’s sperm.
A hermaphrodite (left) and a male (right) of the clam shrimp Eulimnadia texana. Credits to arizonafairyshrimp.com
The persistence of males in the population depends basically on their ability to fertilize hermaphrodites against their will and the sex-determination system of the species. When hermaphrodites produce males by self-fertilization, they are destined to remain for at least some time even if they cannot fertilize that much. Now if self-fertilization only produce hermaphrodites, the poor males have to be really persistent or otherwise they will soon perish.
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References and further reading:
Chasnov JR 2010. The evolution from females to hermaphrodites results in a sexual conflict over mating in androdioecious nematode worms and clam shrimp. Journal of Evolutionary Biology 23: 539–556.
Ellis RE & Schärer L 2014. Rogue Sperm Indicate Sexually Antagonistic Coevolution in Nematodes. PLoS Biol 12: e1001916.
Ford RE & Weeks SC 2018. Intersexual conflict in androdioecious clam shrimp: Do androdioecious hermaphrodites evolve to avoid mating with males? Ethology 124: 357–364.
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