Life cycle matters: DNA barcoding reveals contrasting community structure between fern sporophytes and gametophytes

Abstract

Ferns are the only major lineage of vascular plants that have nutritionally independent sporophyte (diploid) and gametophyte (haploid) life stages. However, the implications of this unique life cycle for fern community ecology have rarely been considered. To compare patterns of community structure between fern sporophytes and gametophytes, we conducted a survey of the ferns of the islands of Moorea and Tahiti (French Polynesia). We first constructed a DNA barcode library (plastid rbcL and trnH‐psbA) for the two island floras including 145 fern species. We then used these DNA barcodes to identify more than 1300 field‐collected gametophytes from 25 plots spanning an elevational gradient from 200 to 2000 m. We found that species richness of fern sporophytes conforms to the well‐known unimodal (i.e., mid‐elevation peak) pattern, reaching a maximum at ~1000–1200 m. Moreover, we found that fern sporophyte communities become increasingly phylogenetically clustered at high elevations. In contrast, species richness of fern gametophytes was consistent across sites, and gametophytes showed no correlation of phylogenetic community structure with elevation. Turnover of sporophyte and gametophyte communities was closely linked with elevation at shallow phylogenetic levels, but not at deeper nodes in the tree. Finally, we found several species for which gametophytes had broader ranges than sporophytes, including a vittarioid fern with abundant gametophytes but extremely rare sporophytes. Our study highlights the importance of including diverse life history stages in surveys of community structure, and has implications for the possible impacts of climate change on the distribution of fern diversity.

Community assembly of the ferns of Florida

“…Nitta et al. (), in the only study of fern community structure to date that has examined both gametophytes and sporophytes, found substantial differences between the two life stages in terms of species composition across sites. This study, like many other studies of fern diversity and community composition (Kluge and Kessler, , ; Watkins Jr. et al., ; Kluge et al., ; Salazar et al., ; Kessler et al., ), focused on changes in species composition and richness over an elevational gradient.…”

“…Nitta et al. () found that the level of phylogenetic clustering differed between the life stages and with elevation, with sporophytes showing evidence of phylogenetic clustering that grew stronger with increasing elevation, while gametophytes showed no evidence of phylogenetic clustering at any elevation. These authors also found, strikingly, that gametophytes showed no evidence of the mid‐elevation peak in species richness that is a hallmark of fern species distributions across elevational gradients in the tropics, based entirely on studies of sporophytes (Cardelus et al., ; Kluge and Kessler, ; Watkins et al., ; Kluge et al., ; Kessler et al., ; Pouteau et al., ).…”

“…Physiologically, for example, ferns have much lower rates of stomatal and hydraulic conductance than most angiosperms (Brodribb and Holbrook, ; Brodribb et al., ; McAdam and Brodribb, ; Martins et al., ), which likely has profound effects on aspects of their habitat and climatic demands that relate to precipitation and water availability. Ferns also have two free‐living, nutritionally and ecologically independent life cycle stages, the sporophyte and gametophyte, each of which may follow its own assembly rules (Haufler et al., ; Nitta et al., ). Ferns have been the subjects of only a handful of community assembly studies (Karst et al., ; Jones et al., ; Kluge and Kessler, ; Hennequin et al., ; Nitta et al., ), and there is reason to suspect that their unique biology may lead to novel assembly patterns.…”

“…Ferns also have two free‐living, nutritionally and ecologically independent life cycle stages, the sporophyte and gametophyte, each of which may follow its own assembly rules (Haufler et al., ; Nitta et al., ). Ferns have been the subjects of only a handful of community assembly studies (Karst et al., ; Jones et al., ; Kluge and Kessler, ; Hennequin et al., ; Nitta et al., ), and there is reason to suspect that their unique biology may lead to novel assembly patterns. While several of these studies have examined the impact of elevational gradients on fern community assembly, our study is the first to investigate the potential effects of spatial scale on analyses of fern species assemblages.…”

What’s ploidy got to do with it? Understanding the evolutionary ecology of macroalgal invasions necessitates incorporating life cycle complexity

“…Angiosperms are "functionally" diplontic because though there is a gametophytic stage, it is few-celled, does not undergo substantial haploid somatic development, and is dependent on the sporophyte. While different ploidies have been compared in angiosperm invasions (Bowen et al, 2017), diploid and polyploid angiosperms are not free-living stages of the same sexual life cycle, but are rather wholly separate life cycles (Wood et al, 2009) In contrast, ferns have dominant sporophytes, and the gametophyte stage (the prothallus) is small and is thought to be rarely seen in nature, but a recent study demonstrated that they are ecologically relevant in which sporophytic and gametophytic communities can differ in species composition and phylogenetic structure (Nitta, Meyer, Taputuarai, & Davis, 2017). Neither the fern gametophyte nor sporophyte is dependent on one another as in mosses or seed plants.…”