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The Evolution of Sexes

Credit: Ezume Images

Credit: Ezume Images

By Jack da Silva

Sex does not depend on the existence of different sexes. Instead, males and females may be the result of genetic conflict arising from the evolution of large and complex individuals.

In the early 1970s, Geoff Parker of The University of Liverpool and colleagues proposed a radical and elegant new theory to explain the evolution of males and females. Then, after some early refinements, the idea settled into a mature theory.

This disruptive selection theory posits that when sexually reproducing organisms become large and complex they benefit from producing large, single-celled embryos that can store nutrients to enable rapid initial development. This provides the opportunity for the evolution of two mating types that produce sex cells of different sizes. One mating type produces many small sex cells that compete for sexual fusions with a second type of individual that produces only a few large sex cells. In the extreme, this results in sperm-producers and egg-producers.

This has been described as the original conflict between the sexes. It is also known as the cost of males, because females make all of the investment in reproduction: a species without sexes would have equal investment from both mating types.

This theory has received some support but has been difficult to distinguish from related competing theories. Recently, however, I derived a specific prediction from a complete mathematical model of the theory and tested it on a group of algae renowned for their cross-species variation in size and complexity. While the test upheld the theory, some exceptions to other predictions of the theory indicate that further refinements to it are necessary.

Sex Without Sexes

The first sexual organisms consisted of single cells that would pair up to fuse into a new single-celled individual with the genetic material of both parent cells. In this new individual, the genetic material of the parents would be shuffled before the cell split into new, genetically unique individuals containing the same amount of genetic material as each parent. The two fusing cells would be outwardly indistinguishable but would belong to different, genetically-determined mating types; that is, two different classes of individuals that could only fuse with members of the other class. In other words, this was sex without sexes.

Things changed, however, when individuals evolved from single cells to multiple cells and then individuals evolved to become larger in size. However, with large individuals there is a growth advantage by producing a large embryo as this allows the storage of more nutrients required in early development. Such natural selection for a large embryo selects, in turn, for large sex cells.

Counterintuitively, this also provides the opportunity for individuals of one mating type to produce many small sex cells rather than a few large ones. This allows them to outcompete individuals of the same mating type for fusions with sex cells of the other mating type. The opportunity to produce many small sex cells arises because the second mating type is then forced to produce fewer, larger sex cells in order to achieve a large embryo.

In its extreme form, one mating type produces many small mobile sex cells and the other produces few, large, non-mobile sex cells. These are what we call males and females.

Thus sexes are borne of genetic conflict, where one genetic type, males, evolved through intense competition for fertilisations of the other genetic type, females, which are consequently forced to invest heavily in their sex cells.

Remarkable Algae

Luckily, single-celled organisms with morphologically indistinguishable sex cells still exist, and one group to which these belong is the algae. These mostly-aquatic plant-like organisms exhibit the whole gamut of structural complexity, from single-celled to complex multicellular individuals. This is fortunate because it allows us to test theories of the evolution of sexes by comparing species of different sizes and levels of complexity.

One intensely studied group, the volvocine green algae, has been especially helpful in this endeavour. These algae have been the focus of attention because they are so diverse, ranging from single-celled species with indistinguishable sex cells (typified by the species Chlamydomonas rheinhardtii) to complex multicellular species with males and females in the genus Volvox.

One prediction from the disruptive selection theory is strongly confirmed in the volvocine algae: that larger species should produce larger single-celled embryos. This is clearly true across all species studied, and even true when considering just single-celled species.

Other predictions are not so strongly confirmed. One of these is that the more complex the organism, the more likely it is to have sex cells that are highly divergent in size. This is broadly true: most single-celled species have indistinguishable sex cells, while the most complex multicellular species have sexes. However, there are single-celled species with males and females, and at least one genus of multicellular species (Astrephomene) that has same-sized sex cells.

Another, similar, prediction is also only partially upheld: that the difference in size between sex cells increases with organism size. This is clearly true for a subset of species, but other species, across a broad range of sizes, have indistinguishable sex cells.

Unresolved Issues

Unanswered questions remain. Why, in apparent contradiction of the disruptive selection theory, do some small single-celled species have sexes while other large, complex species lack any clear distinction between their sex cells? Another unresolved issue is that the predictions outlined above are not specific to the theory; a related class of theories makes the same predictions.

If larger organisms benefit from having larger embryos, and this selects for larger sex cells, then encounter rates between sex cells may increase if one mating type produces many small mobile sex cells while the other produces fewer large sedentary sex cells. The small sex cells may be more efficiently mobile because they are light, and the large sex cells make good targets.

Game Theory

One way forward is to derive a prediction that is specific to the disruptive selection theory. I accomplished this by analysing the most complete mathematical model of the theory available (https://goo.gl/VmTsZ8). The model is based on an approach called game theory. As applied to evolutionary biology, the objective of game theory is to find the optimum evolutionary strategy (e.g. a behaviour, morphology, or any evolved trait of an organism) of each interacting type of individual. In the case of the evolution of sexes, the interacting individuals are the two mating types, and the question is: what size of sex cell should each mating type produce?

It turns out that the strategy of producing smaller sex cells than the other mating type is unbeatable and stable (i.e. it will not revert to the production of same-size sex cells) when the ratio of the size of the larger sex cell to the smaller sex cell is greater than three. If the size difference is smaller than this, the system will revert to the ancestral condition where both mating types produce sex cells of the same size.

I was able to confirm this for the volvocine algae, for which the ratio was greater than 10 for all species that have differences in sex cell size between mating types. Therefore, the evolution of sexes in the volvocine algae is consistent with the disruptive selection theory.

Remaining Mysteries

Although all species of volvocine algae studied so far with different-size sex cells show the predicted ratio of sex cell sizes, there are many large and even complex species that show no difference in the sizes of their sex cells. Members of the genus Astrephomene are examples.

Why don’t some large and complex species evolve sexes? One possibility is that there are constraints on the sizes of sex cells in these species. For example, it may be necessary that both sex cells remain small and highly mobile in order to reach the two-dimensional water surface, where they increase their chances of encountering one another compared with the three-dimensional water column. Or, there may be constraints on the minimum sizes of sex cells. For example, if sex cells have a hard time finding each other, they may need to be big enough to carry sufficient nutrients to survive the time it takes to find a partner. Alternatively, because green algae photosynthesise, both sex cells may need to carry their sunlight-harvesting chloroplasts. This organ takes up most of the space in a volvocine algal cell, thereby severely limiting a cell’s minimum size.

This is an intriguing possibility, since in all algae and plants, the chloroplast is inherited only from one mating type (or the female) and is typically reduced or disintegrated in the smaller sex cell in species with different-sized sex cells. In species with same-sized sex cells, the chloroplast typically remains intact in both sex cells (one chloroplast disintegrates after fusion).

Therefore, one answer to why some large and complex algae do not evolve sexes, in apparent contradiction of the theory, may be that they need to maintain photosynthesis in both sex cells.


Jack da Silva is a senior lecturer in genetics at the University of Adelaide. This article is based on an original research report in Ecology and Evolution (https://goo.gl/vpxoNC).