Museomics Unveil the Phylogeny and Biogeography of the Neglected Juan Fernandez Archipelago Megalachne and Podophorus Endemic Grasses and Their Connection With Relict Pampean-Ventanian Fescues.

María Fernanda Moreno-Aguilar,Itziar Arnelas,Juan Viruel,Aminael Sánchez-Rodríguez,Pilar Catalán

doi:10.3389/fpls.2020.00819

Abstract

Oceanic islands constitute natural laboratories to study plant speciation and biogeographic patterns of island endemics. Juan Fernandez is a southern Pacific archipelago consisting of three small oceanic islands located 600–700 km west of the Chilean coastline. Exposed to current cold seasonal oceanic climate, these 5.8–1 Ma old islands harbor a remarkable endemic flora. All known Fernandezian endemic grass species belong to two genera, Megalachne and Podophorus, of uncertain taxonomic adscription. Classical and modern classifications have placed them either in Bromeae (Bromus), Duthieinae, Aveneae/Poeae, or Loliinae (fine-leaved Festuca); however, none of them have clarified their evolutionary relationships with respect to their closest Festuca relatives. Megalachne includes four species, which are endemic to Masatierra (Robinson Crusoe island) (M. berteroniana and M. robinsoniana) and to Masafuera (Alejandro Selkirk island) (M. masafuerana and M. dantonii). The monotypic Podophorus bromoides is a rare endemic species to Masatierra which is only known from its type locality and is currently considered extinct. We have used museomic approaches to uncover the challenging evolutionary history of these endemic grasses and to infer the divergence and dispersal patterns from their ancestors. Genome skimming data were produced from herbarium samples of M. berteroniana and M. masafuerana, and the 164 years old type specimen of P. bromoides, as well as for a collection of 33 species representing the main broad- and fine-leaved Loliinae lineages. Paired-end reads were successfully mapped to plastomes and nuclear ribosomal cistrons of reference Festuca species and used to reconstruct phylogenetic trees. Filtered ITS and trnTLF sequences from these genomes were further combined with our large Loliinae data sets for accurate biogeographic reconstruction. Nuclear and plastome data recovered a strongly supported fine-leaved Fernandezian clade where Podophorus was resolved as sister to Megalachne. Bayesian divergence dating and dispersal-extinction-cladogenesis range evolution analyses estimated the split of the Fernandezian clade from its ancestral southern American Pampas-Ventanian Loliinae lineage in the Miocene-Pliocene transition, following a long distance dispersal from the continent to the uplifted volcanic palaeo-island of Santa Clara-Masatierra. Consecutive Pliocene-Pleistocene splits and a Masatierra-to-Masafuera dispersal paved the way for in situ speciation of Podophorus and Megalachne taxa.

Highlights

Genomic data are increasingly called upon to elucidate evolutionary and taxonomic challenges posed by several cryptic or ambiguously related organisms, which could not be resolved using traditional approaches, such as morphometrics or standard molecular methods (Harrison and Kidner, 2011; Straub et al, 2012; Carter et al, 2020; Larridon et al, 2020)
Complete and partial plastomes as well as the nuclear rDNA cistron and ITS data supported the phylogenetic placement of the studied Fernandezian Podophorous bromoides, Megalachne berteroniana, and M. masafuerana species within the AmericanVulpia-Pampas fine-leaved Loliinae clade (Figures 2, 3 and Supplementary Figures S1A–C)
Our results corroborate the early suggestions of Tateoka (1962) who indicated a close affinity of Megalachne to Festuca based on shared morphological and serological traits, and the recent phylogenetic findings of Schneider et al (2011, 2012) and Tkach et al (2020) who placed them within the fine-leaved Loliinae, and definitively discard its classification within either Bromeae or Duthieinae

Summary

Introduction

Genomic data are increasingly called upon to elucidate evolutionary and taxonomic challenges posed by several cryptic or ambiguously related organisms, which could not be resolved using traditional approaches, such as morphometrics or standard molecular methods (Harrison and Kidner, 2011; Straub et al, 2012; Carter et al, 2020; Larridon et al, 2020). While the results obtained from the genomic-based approaches are overall congruent with previous findings based on reduced sets of genes and genetic markers (Saarela et al, 2018), the thoroughly dissection of genomes have untapped large sets of taxonomically informative gene copy variants or single nucleotide polymorphism (SNPs) and have allowed the reconstruction of better resolved and more strongly supported phylogenies (Soltis et al, 2018) These new metadata have facilitated the identification of previously neglected cryptic taxa (Spriggs et al, 2019) and the construction of more robust phylogenetic trees where the evolutionary positions of previously unknown, doubtful, or ambiguous lineages have been elucidated in some cases (Leebens-Mack et al, 2019; Li et al, 2019). The combined use of current and extinct plant species samples, and of herbarium and recently collected samples allows to uncover largely sampled phylogenetic trees of plant lineages (Malakasi et al, 2019)

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