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

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.

Digest: Going solo: Self‐fertilization in haploid algae may not lead to evolutionary decline*

“…They found that specialization was less detrimental than expected: only two phylogenies showed significant reduction in diversification and higher “tippiness.” Similarly, Hanschen et al. () show that selfing did not seem to be a dead‐end trait (corroborated by the two reversals from selfing to outcrossing). Bromham et al.…”

“…Hanschen et al. () suspected that certain species have only recently evolved selfing, and descend from outcrossing ancestors. By investigating the evolution of self‐fertilization, they hoped to see how often selfing had evolved, how long it persisted, and if selfing species are concentrated on the tips of the evolutionary tree.…”

“…Hanschen et al. () suggest that these unexpected findings are explained by volvocine algae being mainly haploid over their life cycle, and by the increased benefit of selfing when colonizing new habitats. Haploid organisms have already purged recessive deleterious alleles so they do not suffer the same reproductive costs as diploid organisms due to the absence of inbreeding depression (which arises because homozygosity exposes recessive alleles in diploids).…”

“…Evolution. https://doi.org/ 10.1111/evo.13394.In this issue, Hanschen et al (2017) explored the evolution of selfing in volvocine freshwater algae to test this macroevolutionary theory. In volvocine algae, there are three types of species: monoecious selfing, dioecious selfing, and dioecious outcrossing (Iyengar 1933).…”

“…Because the algae species are facultatively sexual, dioecious selfing species can self-fertilize because the same genotype can develop as male or female (but not both within a single individual). Hanschen et al (2017) suspected that certain species have only recently evolved selfing, and descend from outcrossing ancestors. By investigating the evolution of self-fertilization, they hoped to see how often selfing had evolved, how long it persisted, and if selfing species are concentrated on the tips of the evolutionary tree.…”