When it only takes one to tango: assessing the impact of apomixis in the fern genus Pteris

Abstract

Premise Apomixis (asexual reproduction by seed, spore, or egg) has evolved repeatedly across the tree of life. Studies of animals and angiosperms show that apomictic lineages are often evolutionarily short‐lived and frequently exhibit different distributions than their sexual relatives. However, apomixis is rare in these groups. Less is known about the role of apomixis in the evolution and biogeography of ferns, in which ~10% of species are apomictic. Apomixis is especially common in the fern genus Pteris (34–39% of species); however, because of the limited taxonomic and geographic sampling of previous studies, the true frequency of apomixis and its associations with geography and phylogeny in this lineage remain unclear. Methods We used spore analyses of herbarium specimens to determine reproductive mode for 127 previously unsampled Pteris species. Then we leveraged biogeographic and phylogenetic analyses to estimate the global distribution and evolution of apomixis in Pteris. Results Among all Pteris species examined, we found that 21% are exclusively apomictic, 71% are exclusively sexual, and 8% have conflicting reports. Apomixis is unevenly distributed across the range of the genus, with the Paleotropics exhibiting the highest frequency, and has evolved numerous times across the Pteris phylogeny, with predominantly East Asian and South Asian clades containing the most apomictic species. Conclusions Apomixis arises frequently in Pteris, but apomictic species do not appear to diversify. Species that encompass both apomictic and sexual populations have wider ranges than exclusively sexual or apomictic species, which suggests that sexual and apomictic ferns could occupy separate ecological niches.

Spatial phylogenetics of Japanese ferns: Patterns, processes, and implications for conservation

“…Water limitation is thought to play an important role in promoting apomixis in ferns especially in deserts (Grusz et al, 2021), since ferns depend on water for transfer of sperm to egg, and apomictic plants would be able to reproduce in the absence of water. A similar argument has been made to assert that areas with seasonal monsoons are linked to increased rates of apomixis in ferns (Liu et al, 2012; Tanaka et al, 2014; Picard et al, 2021), but in Japan, although the areas that include high percentages of apomictic taxa are monsoonal, the degree of seasonal water limitation does not approach that of a desert. The monsoon hypothesis was not supported by our results, which showed neither a particularly strong effect of precipitation seasonality in most models (Figure 4), nor a correlation of precipitation seasonality with % apomictic taxa (Appendix S1: Table S2).…”

“…Water limitation is thought to play an important role in promoting apomixis in ferns especially in deserts (Grusz et al, 2021), since ferns depend on water for transfer of sperm to egg, and apomictic plants would be able to reproduce in the absence of water. A similar argument has been made to assert that areas with seasonal monsoons are linked to increased rates of apomixis in ferns (Liu et al, 2012; F I G U R E 6 Phylogenetic endemism of the ferns of Japan measured using categorical analysis of neo-and paleoendemism (CANAPE).…”

“…Bioregions not consisting of more than two grid cells each were lumped into category "Other". Tanaka et al, 2014;Picard et al, 2021), but in Japan, although the areas that include high percentages of apomictic taxa are monsoonal, the degree of seasonal water limitation does not approach that of a desert. The monsoon hypothesis was not supported by our results, which showed neither a particularly strong effect of precipitation seasonality in most models (Figure 4), nor a correlation of precipitation seasonality with % apomictic taxa (Appendix S1: Table S2).…”

Reticulate evolution in the Pteris fauriei group (Pteridaceae)

“…Apogamous hybrid ferns are reported in many cryptic complexes, especially in Aspleniaceae 36 , 37 , Dryopteridaceae 38 – 40 , and Pteridaceae 9 , 28 , 41 . Because apogamous species often have limited genetic variation compared to close sexual relatives 42 , apogamy has been considered a dead end for fern evolution 43 ; however, it is common and could play a special role in Pteris 29 , 44 , 45 , where 21% of species reproduce only by apogamy and 8% of species have both sexual and apogamous individuals. Apogamous gametophytes could produce functional male gametes and serve as paternal parents when crossed with gametophytes of allied sexual species 29 , 46 , 47 .…”

“…Interestingly, apogamous Pteris species are most prevalent in East Asia and South Asia and mostly found in sect. Campteria 45 . The Pteris fauriei group (Pteridaceae), belonging to sect.…”