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, 192 (3), E93-E105

Multicellularity Drives the Evolution of Sexual Traits

Multicellularity Drives the Evolution of Sexual Traits

Erik R Hanschen et al. Am Nat.

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.

Keywords: ancestral state reconstruction; anisogamy; multicellularity; sex; sexual dimorphism; volvocine green algae.

Figures

Figure 1:
Figure 1:
Exemplar species and diversity of sexual systems in the volvocine algae. A, Unicellular Chlamydomonas reinhardtii. B, Undifferentiated Gonium pectorale Russia. C, Undifferentiated Pandorina morum. D, Undifferentiated Eudorina elegans. E, Soma-differentiated Pleodorina californica. F, Germ- and soma-differentiated Volvox carteri f. nagariensis. G, A desiccation-resistant diploid zygospore produces four meiotic products (left) or a reduced number of meiotic products (right). H, Isogamy (equal-sized gametes), anisogamy (unequal sized gametes, with smaller sperm produced by males and larger, flagellated eggs produced by females), and oogamy (unequal sized gametes, unflagellated eggs are much larger than sperm). I, Fertilization external to a multicellular organism versus internal fertilization. J, Female colonies versus extrafertile female colonies, which have at least a twofold increase in reproductive cell number. K, Male colonies with sperm packets versus dwarf male colonies with sperm packets. Cartoons in I–K are shown with Volvox-like morphology for illustrative purposes only.
Figure 2:
Figure 2:
Phylogenetic tree of the volvocine green algae. Numbers indicate Bayesian posterior probabilities (PP). Unlabeled nodes are supported with PP = 1.00. Out-group taxa have been trimmed. Circles show relative metrics of multicellular complexity (number of rounds of cell division, percentage of somatic cells, and body length). A key showing minimum and maximum values of metrics is included. The scale bar (for branch lengths) shows expected substitutions per site.
Figure 3:
Figure 3:
Ancestral state reconstructions of six sexual characters. A, Evolution of all (green) and reduced number of (black) meiotic products germinating from a diploid zygospore. B, Evolution of isogamy (green), anisogamy (blue), and oogamy (black). C, Evolution of external (green) and internal (black) fertilization. D, Evolution of normal females (green) and extrafertile females (black). E, Evolution of normal males (green) and dwarf males (black). For all panels branch color refers to the most likely state inferred by maximum likelihood reconstruction. Pie charts at nodes represent scaled marginal likelihoods from maximum likelihood reconstruction. Dashed branches indicate a statistically ambiguous reconstruction (if the natural logarithm of the ratio of the two likelihoods was less than 2; Pagel 1999). Numbers at select nodes (relevant to the trait in question) indicate Bayes factors (support for that character state against the next most likely state), colored by which state is most strongly supported. Interpretation of Bayes factors (Kass and Raftery 1995) is as follows: 0–2, barely worth mentioning; 2–6, positive; 6–10, strong; and >10, very strong.
Figure 4:
Figure 4:
Relationships between the number of derived sexual traits in each species (not including multicellular sperm packets, which are perfectly correlated with anisogamy) and three traits related to multicellular complexity: the number of rounds of cell division in that species (A), the percentage of somatic cells (B), and natural logarithm–transformed body length. Relative sizes of the data points (tips of the phylogeny) are scaled to indicate the number of species at that coordinate (from 1 to 15). Phylogenetic regression lines and statistics (red) and simple linear regressions and statistics (blue) are shown.

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