The Origins of Two Sexes
The Origins of Two Sexes
Humans are a species with precisely two sexes, no more and no less.
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This article was originally published on the author’s website, The Paradox Institute, on April 4, 2022.
Humans are a species with precisely two sexes, no more and no less. This means that there are exactly two distinct reproductive roles—referred to as male and female—centered around the production of two gametes of differing size (a form of sexual reproduction known as anisogamy). The two reproductive roles of male and female are biological categories, and they are defined the same across a vast array of species:
The male sex is the phenotype that produces many small, motile gametes (sperm), and the female sex is the phenotype that produces few large, sessile gametes (ova).
Because male and female are fundamentally defined by the gametes they produce, understanding the origins of the two sexes means understanding why gametes come in two different sizes—many small motile ones (sperm) and few large sessile ones (eggs). Thus, we must trace the sexes all the way back to the origins of gametes—the primary biological vehicles through which sexual reproduction takes place.
Sexual reproduction is the mixing of genomes and the fusion of gametes, a process which forms a new genetically unique individual.[1] It first arrived on the scene around two billion years ago with single-celled eukaryotic organisms.[2] Despite heavy evolutionary costs, the stronger evolutionary advantages from sexual reproduction made it near universal among eukaryotes, with now more than 99.9% of named animal species reproducing sexually.[3]
Sex Before the Two Sexes
Two billion years ago, however, sexual reproduction occurred in the absence of males and females. In fact, it might seem paradoxical, but sexual reproduction is entirely possible without the existence of the sexes. Between one and two billion years ago, sexual reproduction largely occurred—not through the fusion of gametes of different size and form (sperm and egg)—but through the fusion of gametes that were equal in size. This form of sexual reproduction is known as isogamy (iso = equal; gamos = marriage); it was and still is most common among unicellular organisms, some types of multicellular algae, and fungi.[4]
Isogamy occurs when all gametes are morphologically similar, particularly in size, and when the contribution of genetic material and resources to the zygote is shared equally between the two parents.[5] During isogamous reproduction among organisms like algae, gametes are released into the sea, meet and fuse, and undergo nuclear fusion to form the new zygote.[6]
Gamete compatibility (which sex cells can fuse with each other) is determined by molecular mechanisms that act as lock and key systems known as mating types.[7] Isogamous organisms like fungi can sometimes have thousands of mating types (thousands of pairs of locks and keys), providing a large set of gametes each similar in size yet different on the molecular level.
This huge number of mating types does not change the fundamental feature of sex, however. Even in isogamous systems, where gametes are the same size, mating is asymmetric: gamete fusions are always between different types. There has never been a documented species where every gamete can fuse with any other gamete.[8]
With mating types in place, requiring different gamete genotypes for fusion, the stage was set for the emergence of male and female sexes. All that was needed was a divergence of gametes from similar sizes and into different sizes and forms.
From Isogamy to Anisogamy
Over hundreds of millions of years, eukaryotes continued to evolve and become more complex, and as the number of cells increased, so did organisms’ adult body sizes. This increase in multicellular complexity necessitated more resources to be provided for each developing zygote.[9] And this increased demand for resources necessitated larger gamete sizes. Thus, as organisms became larger, so did their gametes.[10]
As the gametes became larger, however, a major problem began to arise: though they contributed heavily to the zygote’s survival and growth through the provision of large amounts of material, the gametes themselves were slower, heavier, and fewer in number, becoming less efficient at finding and fusing with one another.
However, with the zygote’s increased body size and multicellular complexity, it still needed many resources to survive and develop, and this meant gamete sizes had to stay large. At the same time, the efficiency of the sexual system (such as the number of gamete fusions) had to be maintained to continue the lineage of the species. This meant that, for the most efficient system, gametes would have to be simultaneously large and few in number with many resources (for the zygote’s survival) and small and numerous with much less resources (for the maximum number of fast gamete fusions).
Thus, the dual problem is evident: how do you increase the efficiency of the sexual system without decreasing zygote fitness? The answer was found through a process known as disruptive selection, where the best evolutionary solution is in the extremes.[11]
Through disruptive selection, some gametes grew smaller and increased in number, trading the large amount of resources for the advantage of speed and quantity, while other gametes grew larger and decreased in number, trading the potential for speed and number for the advantage of size and robustness.[12] Finally, some unfortunate gametes found themselves stuck in the middle: they neither had the maximum speed and number nor the maximum size and robustness. Their reproductive fitness was beaten by both the many fast motile gametes and the few large sessile gametes. Thus, the intermediate gamete sizes soon went extinct, leaving the two most optimal sizes in their place.
As developmental biologist Emma Hilton writes:
What rapidly emerges as the most efficient system—one that maximizes the number of successful collisions while maintaining robustness of offspring—comprises two types of gamete. The two gamete types that permit maximal reproductive efficiency are:
1) One slow/stationary large target that confers all the robustness to the offspring.
2) Multiple small, fast missiles peppering the target.
The possibility of multiple gamete sizes and multiple ways of conferring robustness are quickly weeded out as the system collapses into two extremes that represent optimum function.
This system of two gametes of differing size and form, with unequal contribution of resources to the zygote from the two parents, is known as anisogamy (aniso = unequal; gamos = marriage). After gametes diverge into two extremely different sizes through disruptive selection, it is near impossible to reverse it. Reversing this development would require exceptional circumstances, such as a reversal of organismal complexity.[13]
Thus, the development of gametes into two different sizes and forms is mostly a one-way path, and because of the reproductive optimality—balancing out the disadvantages of the two gamete types through divergence into both extremes—anisogamy has become the dominant system of sexual reproduction across the plant and animal kingdoms.[14]
The Emergence of Two Sexes
Once the gametes have diverged into two different sizes and become stable, two sexes are formed—no more and no less.[15] With two different gametes (few large sessile ones and many small motile ones) two different reproductive roles are generated, along with the evolution of reproductive anatomy for the production and release of the sex-specific gamete type.
Thus, the sex-based differences between males and females, particularly the differences in reproductive anatomy and the subsequent impacts of natural and sexual selection on body type and behavior, can be traced back to the divergence of gametes into those two different sizes.
The evolution of gametes into two extremes, and the subsequent emergence of two sexes, is so optimal for sexual reproduction that the male-female dichotomy has “evolved independently across nearly all lineages of multicellular organisms.”[16] In fact, evolutionary biologists reiterate that the divergence into two sexes is “an almost inevitable consequence of sexual reproduction.”[17]
Organizations to Support
References:
[1] Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman TL, et al. (2014). Sex Determination–Why So Many Ways of Doing It. PLoS Biol, 12(7).
[2] Otto, S. (2008). Sexual reproduction and the evolution of sex. Nature Education, 1(1), 182; A eukaryote is any cell or organism that possesses DNA in the form of chromosomes contained within a clearly defined nucleus. It includes all living organisms other than eubacteria and archaebacteria.
[3] Otto, S. (2009). The evolutionary enigma of sex. The American Naturalist, 174(S1), 1-14; Vrijenhoek, R. C. (1998). Animal clones and diversity. BioScience, 48, 617-628.
[4] Kirk, D. (2006). Oogamy–inventing the sexes. Current Biology, 16(24).
[5] Lehtonen, J., Kokko, H., Parker, GA. (2016). What do isogamous organisms teach us about sex and the two sexes? PTBS, 371(1706), 2.
[6] Ibid., 3.
[7] Perrin, N. (2011). What uses are mating types? The ‘developmental switch’ model. Evolution, 66-4, 947-956.
[8] Czaran, T., Hoekstra. R. (2004). Evolution of sexual asymmetry. BMC Evolutionary Biology, 4(34).
[9] da Silva, J. (2018). The evolution of sexes–a specific test of the disruptive selection theory. Ecology and Evolution, 8, 207; Lehtonen, J., Parker, G. (2014). 1165.
[10] Lehtonen, J., Parker, G. (2014). Gamete competition, gamete limitation, and the evolution of the two sexes. Molecular Human Reproduction, 1165.
[11] Parker et al. (1972); Bell 1978; Hoekstra (1982); Bulmer and Parker (2002).
[12] da Silva, J. (2018).
[13] Lehtonen, J., Parker, G. (2014). 1165.
[14] Iwasa & Sasaki (1987); Kodric-Brown & Brown (1987); Czaran & Hoekstra (2004); Epelman et al. (2005); Lehtonen, J., Parker, G. (2014). 1162; Parker, GA. (2014); Lehtonen, Kokko, and Parker (2016); Lehtonen & Parker (2019).
[15] Lehtonen, J., Parker, G. (2014). 1162.
[16] Kirk, D. (2006). Oogamy–inventing the sexes. Current Biology, 16(24).
[17] Lehtonen, J., Parker, G. (2014). 1161.
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