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. 2018 Feb;72(2):386-398.
doi: 10.1111/evo.13394. Epub 2017 Nov 24.

Repeated evolution and reversibility of self-fertilization in the volvocine green algae

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Repeated evolution and reversibility of self-fertilization in the volvocine green algae

Erik R Hanschen et al. Evolution. 2018 Feb.

Abstract

Outcrossing and self-fertilization are fundamental strategies of sexual reproduction, each with different evolutionary costs and benefits. Self-fertilization is thought to be an evolutionary "dead-end" strategy, beneficial in the short term but costly in the long term, resulting in self-fertilizing species that occupy only the tips of phylogenetic trees. Here, we use volvocine green algae to investigate the evolution of self-fertilization. We use ancestral-state reconstructions to show that self-fertilization has repeatedly evolved from outcrossing ancestors and that multiple reversals from selfing to outcrossing have occurred. We use three phylogenetic metrics to show that self-fertilization is not restricted to the tips of the phylogenetic tree, a finding inconsistent with the view of self-fertilization as a dead-end strategy. We also find no evidence for higher extinction rates or lower speciation rates in selfing lineages. We find that self-fertilizing species have significantly larger colonies than outcrossing species, suggesting the benefits of selfing may counteract the costs of increased size. We speculate that our macroevolutionary results on self-fertilization (i.e., non-tippy distribution, no decreased diversification rates) may be explained by the haploid-dominant life cycle that occurs in volvocine algae, which may alter the costs and benefits of selfing.

Keywords: Haploid; phylogenetics; self-fertilization; sex; sexual reproduction; volvocine green algae.

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Figures

Figure 1
Figure 1
Diversity of mating systems in the volvocine green algae and their respective life cycles. A. In outcrossing (heterothallic) species, distinct genotypes (male on left and female on right) sexually differentiate producing either eggs or sperm. A diploid zygospore (red) is produced after fertilization. Sexual offspring hatch and enter the haploid, asexual phase of the life cycle. B. In selfing (homothallic) monoecious species, a single genotype is capable of producing both gamete types. Upon sexual differentiation, each sexual colony produces both sperm and eggs. C. In selfing (homothallic) dioecious species, a single genotype sexually differentiates, producing either eggs or sperm, but not both within the same colony. Cartoons in panels A–C are shown with anisogamous, Volvox-like morphology for illustrative purposes only.
Figure 2
Figure 2
Ancestral state reconstruction of selfing (left) and monoecy (right). Left, the evolution of outcrossing (black) and selfing (green). Right, the evolution of dioecy (black, for this analysis, outcrossing heterothallic species were treated as dioecious) and monoecy (blue). Three selfing species (Tetrabaena socialis, Gonium pectorale Russia, Gonium multicoccum UTEX 2580) break apart into unicells during sexual differentiation preventing assignment to monoecy or dioecy. Branch color refers to the most likely state inferred by maximum likelihood (ML) reconstruction. Pie charts at nodes represent scaled marginal likelihoods from ML reconstruction. Numbers at select nodes indicate Bayes factors (support for that character state against the next most likely state), which explicitly take phylogenetic uncertainty into account, colored by which state is most supported. Interpretation of Bayes factors (Kass and Raftery 1995): 0 to 2 barely worth mentioning, 2 to 6 positive, 6 to 10 strong,>10 very strong. Chlamy, Chlamydomonas; Astre, Astrephomene; Col., Colemanosphaera; N., NIES; U., UTEX.
Figure 3
Figure 3
Summary of the number of observed transitions between mating systems. This minimum number of transitions was counted after assigning each ancestor to the most likely state. We treated the origin of selfing in Pleodorina japonica, Pleodorina californica, and Volvox aureus as one transition, although the ancestral state of the ancestor to these three species is ambiguous. Three homothallic species break apart into unicells during sexual differentiation preventing assignment to monoecy or dioecy (unknown-ecious homothallism).
Figure 4
Figure 4
Quantification of "tippiness" of homothallic self-fertilization across the volvocine phylometric tree. A. Sum of sister clade differences, which measures trait clustering by assigning tips (species) the value 0 or 1, assigning each node the absolute difference of the two daughter tip/nodes, then summing across all nodes. B. Tip age rank sum, which compares the branch length associated with tips (species) for each state. C. Number of tips per origin, which compares the observed number of tips per origin of the trait to a Brownian motion null model with the same trait frequency among species as in the observed data. For all panels, the histogram represents a null distribution calculated from 1,000,000 simulations of a threshold Brownian motion model with the same trait frequencies as in the observed data (red line). This analysis was repeated with an ultrametric tree (Fig. S3), which gave very similar results.

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