On the widespread capacity for, and functional significance of, extreme inbreeding in ferns

Abstract

SummaryHomosporous vascular plants utilize three different mating systems, one of which, gametophytic selfing, is an extreme form of inbreeding only possible in homosporous groups. This mating system results in complete homozygosity in all progeny and has important evolutionary and ecological implications. Ferns are the largest group of homosporous land plants, and the significance of extreme inbreeding for fern evolution has been a subject of debate for decades.We cultured gametophytes in the laboratory and quantified the relative frequencies of sporophyte production from isolated and paired gametophytes, and examined associations between breeding systems and several ecological and evolutionary traits.The majority of fern species studied show a capacity for gametophytic selfing, producing sporophytes from both isolated and paired gametophytes. While we did not follow sporophytes to maturity to investigate potential detrimental effects of homozygosity at later developmental stages, our results suggest that gametophytic selfing may have greater significance for fern evolution and diversification than has previously been realized.We present evidence from the largest study of mating behavior in ferns to date that the capacity for extreme inbreeding is prevalent in this lineage, and we discuss its implications and relevance and make recommendations for future studies of fern mating systems.

Sex and the Single Gametophyte: Revising the Homosporous Vascular Plant Life Cycle in Light of Contemporary Research

“…The facts are clear: Studies of ferns reveal that most are characterized by the capacity for both inbreeding and outcrossing and quite effectively maintain the genetic diversity necessary for long-term evolutionary success (reviewed by Sessa et al 2016).…”

“…At the other end of the spectrum, some species are obligate outcrossers and have redundant mechanisms to promote such a breeding system (e.g., Haufler and Soltis 1984). Recent work has shown that most homosporous ferns (up to 70% of the species examined) are capable of initiating sporophyte progeny in vitro via gametophytic selfing as well as via sporophytic selfing or sporophytic outcrossing (Sessa et al 2016). Demonstrating such mating system flexibility in laboratory cultures highlights crucial options that may be exploited in nature to maximize success in the face of varying ecological conditions.…”

“…For example, Nephrolepis exaltata appears to have little to no genetic load (Lloyd 1974a) and is a pioneer species that is one of the first to establish on recent lava flows. The majority of fern species analyzed through in vitro gametophyte culture demonstrate a capacity for gametophytic selfing (Sessa et al 2016) that would potentially allow them to colonize new habitats via this means (depending on the amount of genetic load). Through somatic mutation or with the arrival of additional spores, these species can subsequently exploit sporophytic selfing or even sporophytic outcrossing (figure 1) to enhance genetic variability.…”

“…Similar studies of fern populations have demonstrated that very few have the depauperate genetic profiles expected of plants with a history of significant gametophytic selfing Soltis DE 1990, Soltis DE andSoltis PS 1992). More recent, broader-scale analyses of sexual gametophytes grown in vitro indicate that about 64% of the nearly 100 species investigated were capable of both gametophytic and sporophytic selfing (see figure 1), whereas 32% only produced sporophytes via crossing between gametophytes (either sporophytic selfing or sporophytic outcrossing) and only about 4% engaged exclusively in gametophytic selfing (Sessa et al 2016). The potential for such mixed-mating systems in ferns highlights their flexibility and may allow them to establish new populations through single spore dispersal (via gametophytic selfing) while simultaneously maintaining significant genetic variation (via sporophytic selfing or sporophytic outcrossing).…”

Two Beringian Origins for the Allotetraploid Fern Polystichum braunii (Dryopteridaceae)

“…A single fern spore can travel a great distance to a new habitat, germinate to yield a gametophyte, and produce a sporophyte via gametophytic selfing (e.g. de Groot et al 2012;Sessa et al 2016). Hence, allopolyploid ferns combine increased capacity for selfing and the built-in genetic diversity inherent in their origins with the unusual dispersal capacity of spore-dispersed plants.…”