Origins of the fern genus Hymenophyllum (Hymenophyllaceae) in New Caledonia: Multiple independent colonizations from surrounding territories and limited in situ diversification

Abstract

Based on a worldwide dataset of molecular sequence data from three plastid DNA markers (rbcL, rbcL-accD-accD, rps4-trnS) obtained from 109 species of Hymenophyllum (Hymenophyllaceae), we investigated the systematics and biogeographic origins of the New Caledonian (NC) members of this fern genus, which were thought to include 16 species with 10 endemics. Located in the southwest Pacific, NC is a continental Gondwanan island that was long supposed to harbour phylogenetic relicts. However, molecular and geological data suggest that the current flora and fauna are the result of recent colonizations that occurred after total submersion (during the Eocene) and subsequent re-emersion of NC ca. 37 Ma. Our molecular phylogenetic results, complemented by morphological observations of herbarium specimens, show the existence of a new species that was as yet undescribed, and suggest that a previously recognized variety should be elevated to the rank of species to avoid species polyphyly. These two species, which are recognizable based on several morphological features, are endemic to NC: (i) Hymenophyllum soriemersum sp. nov. is sister to the other NC endemic H. dimidiatum; and (ii) H. neocaledonicum comb. & stat. nov, previously described as a variety within H. lyallii, was retrieved as a distinct lineage. We also confirmed the synonymy of H. streptophyllum and H. subdimidiatum (both previously considered as endemic to NC) with the more widely distributed H. javanicum and H. holochilum, respectively. These synonymies were previously hypothesised based on morphology alone. New Caledonia thus has as total of 17 Hymenophyllum species, 12 (71%) of which are endemics. Biogeographic inferences based on the results of our phylogenetic analyses suggest that Hymenophyllum originated in New Zealand ca. 49.8 Ma (95% HPD: 40.7-59.5 Ma). Its spatio-temporal history may in part have been influenced by vicariance (with potential exchange via the Antarctica land bridge that persisted between Australia and South America until 34 Ma), but long-distance dispersal (LDD) appears as the predominant process leading to the present-day distribution of species. At least eight LDD events are needed to explain the presence of the 10 NC endemics analysed here (H. francii and H. humboldtianum were not included), each of which occurred < 22.1 Ma and originated from a surrounding territory: Southeast Asia was probably the dispersal source for the NC endemic clade comprising H. soriemersum, H. dimidiatum, and H. rolandi-principis while the ancestors of the other NC endemics most likely dispersed from New Zealand, Australia or other Pacific Islands. Such a regional pattern is congruent with the distribution of non-endemic species, which are mostly shared among neighbouring territories. Lastly, we found evidence for only two cases of diversification within NC, yielding two and three species each (H. soriemersum, H. dimidiatum and H. rolandi-principis; and H. lyallii and the ancestor of H. braithwaitei and H. tomaniiviense). Such a low level of in situ di...

Going under down under? Lineage ages argue for extensive survival of the Oligocene marine transgression on Zealandia

“…In mite harvestmen once again, at least 26 lineages (enlarged in number by in situ speciation) are claimed to have survived through the OMT: Rakaia [16], Aoraki [9] and Neopurcellia [1] (Giribet et al., ). For Hymenophyllum ferns (Del Rio et al., ) and Schistochila liverworts (Sun et al., ), slowly evolving cpDNA suggests that at least 13 and 9–10 lineages, respectively, survived the NZ OMT. Two lineages of ground weta, tusked weta and possibly tree/giant weta, appear to have survived in situ (Pratt et al., ; Trewick & Morgan‐Richards, ).…”

A global plastid phylogeny of the fern genus Asplenium (Aspleniaceae)

“…(Polypodiaceae) in the Hawaiian islands (Sundue et al., ), and a few species of Hymenophyllum Sm. (Hymenophyllaceae) on New Caledonia (Del Rio et al., ).…”

Recent advances in New Caledonian biogeography

“…Analyses using S‐DIVA and DEC models both supported New Zealand as the most likely ancestral area of the genus (Del Rio et al, ). However, this result simply reflects the tendency of both algorithms to interpret the region occupied by a basal paraphyletic grade as a centre of origin.…”

“…The filmy fern Hymenophyllum has a cosmopolitan distribution and comprises three main clades (Del Rio et al, ): New Zealand, New Caledonia and southern Chile. (Subg.…”