Plastid Phylogenomics Resolve Deep Relationships among Eupolypod II Ferns with Rapid Radiation and Rate Heterogeneity

Abstract

The eupolypods II ferns represent a classic case of evolutionary radiation and, simultaneously, exhibit high substitution rate heterogeneity. These factors have been proposed to contribute to the contentious resolutions among clades within this fern group in multilocus phylogenetic studies. We investigated the deep phylogenetic relationships of eupolypod II ferns by sampling all major families and using 40 plastid genomes, or plastomes, of which 33 were newly sequenced with next-generation sequencing technology. We performed model-based analyses to evaluate the diversity of molecular evolutionary rates for these ferns. Our plastome data, with more than 26,000 informative characters, yielded good resolution for deep relationships within eupolypods II and unambiguously clarified the position of Rhachidosoraceae and the monophyly of Athyriaceae. Results of rate heterogeneity analysis revealed approximately 33 significant rate shifts in eupolypod II ferns, with the most heterogeneous rates (both accelerations and decelerations) occurring in two phylogenetically difficult lineages, that is, the Rhachidosoraceae–Aspleniaceae and Athyriaceae clades. These observations support the hypothesis that rate heterogeneity has previously constrained the deep phylogenetic resolution in eupolypods II. According to the plastome data, we propose that 14 chloroplast markers are particularly phylogenetically informative for eupolypods II both at the familial and generic levels. Our study demonstrates the power of a character-rich plastome data set and high-throughput sequencing for resolving the recalcitrant lineages, which have undergone rapid evolutionary radiation and dramatic changes in substitution rates.

Chloroplast phylogenomic data support Eocene amphi‐Pacific early radiation for the Asian Palmate core Araliaceae

“…The application of the NGS techniques has enabled access to large amounts of data and has helped resolve the basal polytomies in certain groups of organisms where traditional Sanger approaches using analyses of multiple‐genes failed (e.g., Graminoids, Leseber & Duvall, ; Rhinoceroses, Willerslev et al, ; Pentapetaleae, Moore et al, ; Paserida, Nabholz et al, ; Neoaves, Pacheco et al, ; Malpighiales, Xi et al, ; Commelinids, Barrett et al, ; Guenons, Guschanski et al, ; Zingiberales, Barrett et al, , Sass et al, ; Ipomeeae, Eserman et al, ; Arundinarieae, Ma et al, ; Apocynaceae, Straub et al, ; Asteraceae, Mandel et al, ; Goodeniaceae, Gardner et al, ; Columbiforms, Soares et al, ; Vitales, Zhang et al, , Wen et al, ; Eupolypod II Ferns, Wei et al, ; Hippeastreae, García et al, ; Protea , Mitchell et al, ). Most of these studies concluded in favor of the radiation hypothesis, since the NGS analysis of complete chloroplast genomes and large nuclear data sets yielded short deep branches (Leseber & Duvall, ; Moore et al, ; Nabholz et al, ; Xi et al, ; Guschanski et al, ; Straub et al, ; Mandel et al, ; Gardner et al, ; Sass et al, ; Soares et al, ; Zhang et al, ; García et al, ; Mitchell et al, ) or non‐fully resolved trees (Willerslev et al, ; Barrett et al, , ; Ma et al, ; Wei et al, ). A previous phylogenetic study based on seven DNA regions proposed a burst of diversification for the origin of the Asian Palmate group (Valcárcel et al, ).…”

Pteridryaceae: A new fern family of Polypodiineae (Polypodiales) including taxonomic treatments

“…Therefore, the sister relationship between the DMPP clade and the remaining Tectariaceae s.l., in spite of the largest character and taxon sampling applied to this question so far, remains uncertain, which is unique for any families of lycophytes and ferns recognized in the classification proposed by PPG I (). Even Athyriaceae, sometimes not strongly supported as monophyletic (e.g., Rothfels et al, ), have been strongly supported to be monophyletic recently (Wei et al, ).…”

Comparative Analysis of the Complete Chloroplast Genome of the Alloplasmic Sunflower (Helianthus L.) Lines with Various CMS Types

“…It was shown that the rpo genes are highly variable and reliable phylogenetic markers, effective in the reconstruction of interrelations of species belonging to the same genus (Krawczyk and Sawicki 2013). A high level of polymorphism of ndh, rpoC2, rbcL and ycf1 genes is also demonstrated in other studies (Wei et al, 2017;Joseph et al, 2013;Benkeblia, 2014).…”