“Multicellularity drives the evolution of sexual traits”

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Erik R. Hanschen, Matthew D. Herron, John J. Wiens, Hisayoshi Nozaki, and Richard E. Michod (Sep 2018)

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Multicellularity causes the evolution of sexual traits including anisogamy

One of the largest volvocine green algae, Volvox carteri, has sexually dimorphic males and females.
(Credit: Erik Hanschen)

Sex didn’t always involve males and females. In fact, sex existed before males and females, and many species are still doing it without them. Males and females are defined by the different sizes of gametes they produce, and not all species produce two different sizes of gametes. Why sperm-producing males and egg-producing females evolved from ancestors without differentiated gametes is a major problem in evolutionary biology. Work led by Erik Hanschen that involved scientists at the University of Arizona, Georgia Tech, and the University of Tokyo suggests that the evolution of large, multicellular bodies drove the evolution of male and female sexes. Using the volvocine green algae to test mathematical theory dating back to the 1970s, they showed a positive relationship between body size and derived sexual characters, starting with different sized gametes (sperm and eggs). Larger species are more likely to have internal fertilization, as in mammals, while smaller species have external fertilization, as in most fishes. Body size is also related to the evolution of secondary sexual dimorphism, differences between males and females of the same species beyond their gametes. As in many birds, mammals, and other animals, male and female individuals of some large volvocine algae differ in their physical characteristics. The convergence of these patterns between the volvocine algae and other taxa suggests that the same principles apply to the evolution of the sexes in other groups, including plants and animals. The evolution of males and females, and subsequently of secondary sexual dimorphism, may be an inevitable consequence of the evolution of large, multicellular bodies.


Abstract

From the male peacock’s tail plumage to the floral displays of flowering plants, traits related to sexual reproduction are often complex and exaggerated. Why has sexual reproduction become so complicated? Why have such exaggerated sexual traits evolved? Early work posited a connection between multicellularity and sexual traits such as anisogamy (i.e., the evolution of small sperm and large eggs). Anisogamy then drives the evolution of other forms of sexual dimorphism. Yet, the relationship between multicellularity and the evolution of sexual traits has not been empirically tested. Given their extensive variation in both multicellular complexity and sexual systems, the volvocine green algae offer a tractable system for understanding the interrelationship of multicellular complexity and sex. Here we show that species with greater multicellular complexity have a significantly larger number of derived sexual traits, including anisogamy, internal fertilization, and secondary sexual dimorphism. Our results demonstrate that anisogamy repeatedly evolved from isogamous multicellular ancestors and that anisogamous species are larger and produce larger zygotes than isogamous species. In the volvocine algae, the evolution of multicellularity likely drives the evolution of anisogamy, and anisogamy subsequently drives secondary sexual dimorphism. Multicellularity may set the stage for the overall diversity of sexual complexity throughout the Tree of Life.