The Evolutionary Dynamics of Apomixis in Ferns: A Case Study from Polystichoid Ferns

The disparate distribution of apomixis between the major plant lineages is arguably one of the most paradoxical phenomena in plant evolution. Ferns are particularly interesting for addressing this issue because apomixis is more frequent than in any other group of plants. Here, we use a phylogenetic framework to explore some aspects of the evolution of apomixis in ferns and in particular in the polystichoid ferns. Our findings indicate that apomixis evolved several times independently in three different clades of polystichoid ferns. A lineage-wide perspective across ferns indicates a correlation between apomixis and the species richness of lineages; however BiSSE tests did not recover evidence for a correlation of apomixis and diversification rates. Instead, evidence was recovered supporting an association between the establishment of apomixis and reticulate evolution, especially in the establishment of triploid hybrids. Diversification time estimates supported the hypothesis of short living apomictic lineages and indicated a link between the establishment of apomixis and the strengthening of the monsoons caused by the lifting of the Qinghai-Tibetan plateau. In general our results supported the hypothesis for the rare establishment of apomictic lineages, high extinction risks, and low speciation rates. 1. Introduction The evolution of asexual reproduction in multicellular eukaryote lineages such as animals, fungi, and plants continues to attract the interests of biologists [1–3]. The prevalence of sexual reproduction in these lineages is paradoxical considering the theoretical advantages associated to asexual reproduction [3, 4]. Hypotheses to explain this paradox have concerned lower rates of speciation and higher rates of extinction in asexual lineages. Essentially, the short-term ecological advantages of asexual reproduction are balanced by the long-term effect of lower diversification rates. This hypothesis is consistent with reported evidence for short-lived apomictic lineages, for example, the derived fern genus Astrolepis [5], and the developmental feature changes required for the loss of sexuality in plants [3]. However, it is inconsistent with other studies that recover evidence for species rich lineages that lack any reported evidence for at least rare sexual events [6, 7], and a recent study on the eudicot genus Oenothera, which shows “increasing diversification associated with loss of sexual recombination and segregation” [4]. This conflicting evidence questions our general understanding of the evolution of asexual reproduction, and the