Multicellularity Drives the Evolution of Sexual Traits

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.

Superorganismal anisogamy: queen–male dimorphism in eusocial insects

“…Models of anisogamy evolution under gamete competition make testable predictions, some of which apply to the current model. A prediction that is transferrable to the current model is that gamete dimorphism is predicted to increase with increasing size and complexity of the adult organism [12,17,43], and this prediction has some empirical support from comparative studies [44][45][46]. In the superorganism model, the analogous prediction is that queen-male dimorphism is predicted to increase with increasing size (i.e.…”

Volvox and volvocine green algae

“…The late David Kirk, whose laboratory played a major role in ushering Volvox research into the modern molecular era, summarized 12 key steps or innovations in the progression from a unicellular Chlamydomonas-like ancestor to V. carteri [21] (summarized in Fig. 1, with subsequent refinement/elaboration by others [5,23,24]). The earliest innovations include cell adhesion, genetic control of cell number, acquisition of organismal polarity, incomplete cytokinesis with formation of cytoplasmic bridges between embryonic blastomeres,…”

“…As described above, Volvox has separate male and female sexes whose differentiation is controlled by a pair of haploid UV sex chromosomes [12] that evolved from an ancestral mating-type locus [10,11] The entire volvocine lineage has been used as a test case for predictions about how/why anisogamy and oogamy evolved in response to an increase in organismal size and cell number [10,24]. The conserved RWP-RK family transcription factor, Mid (minus dominance) resides on the male chromosome (or minus matingtype locus in isogamous species) and controls male or minus sexual differentiation in dioicous species of volvocine algae [10].…”

“…This finding and others fit predictions of evolutionary theory [40] where sex chromosomes are postulated to acquire genes required for reproductive fitness of males or females. Other derived aspects of the Volvox sexual cycle such as SI-triggered signal transduction, internal fertilization, and reduced meiotic products are fascinating and relatively unexplored areas of interest [10,24].…”

Transmissible cancer and the evolution of sex

“…Although sexual processes undoubtedly antedated multicellularity, no successful transition to multicellularity (i.e., when cancer emerged [33]) has avoided a tight connection with the sexual process [39,40]. Multicellularity may even set the stage for the overall diversity of sexual complexity throughout the Tree of Life [41].…”