Abstract

In the age of next-generation sequencing, the number of loci available for phylogenetic analyses has increased by orders of magnitude. But despite this dramatic increase in the amount of data, some phylogenomic studies have revealed rampant gene-tree discordance that can be caused by many historical processes, such as rapid diversification, gene duplication, or reticulate evolution. We used a target enrichment approach to sample 400 single-copy nuclear genes and estimate the phylogenetic relationships of 13 genera in the lichen-forming family Lobariaceae to address the effect of data type (nucleotides and amino acids) and phylogenetic reconstruction method (concatenation and species tree approaches). Furthermore, we examined datasets for evidence of historical processes, such as rapid diversification and reticulate evolution. We found incongruence associated with sequence data types (nucleotide vs. amino acid sequences) and with different methods of phylogenetic reconstruction (species tree vs. concatenation). The resulting phylogenetic trees provided evidence for rapid and reticulate evolution based on extremely short branches in the backbone of the phylogenies. The observed rapid and reticulate diversifications may explain conflicts among gene trees and the challenges to resolving evolutionary relationships. Based on divergence times, the diversification at the backbone occurred near the Cretaceous-Paleogene (K-Pg) boundary (65 Mya) which is consistent with other rapid diversifications in the tree of life. Although some phylogenetic relationships within the Lobariaceae family remain with low support, even with our powerful phylogenomic dataset of up to 376 genes, our use of target-capturing data allowed for the novel exploration of the mechanisms underlying phylogenetic and systematic incongruence.

Highlights

  • With the advent of next-generation sequencing (NGS) technology, the evolutionary relationships of many groups on the tree of life are increasingly resolved and our understanding of the diversification of these groups has been significantly improved[1,2,3]

  • Most coverage was achieved for Lobaria pulmonaria which was used as the reference in HybPiper and for the bait design

  • The trees produced after running the HybPiper script paralog_retriever. py to obtain all paralogous sequences for all flagged loci exhibited two patterns: (1) the two sequences retrieved would cluster and form a clade or (2) the two sequences would be resolved in two very different clades, separated by a long branch, which is indicative of an ancestral gene duplication event but could be explained by allopolyploid hybridization

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Summary

Introduction

With the advent of next-generation sequencing (NGS) technology, the evolutionary relationships of many groups on the tree of life are increasingly resolved and our understanding of the diversification of these groups has been significantly improved[1,2,3]. Nucleotide data can suffer from substitutional saturation at particular sites in a genome[22] Such homoplasy is difficult to model in tree reconstruction methods and result in phylogenetic signatures being erased[23]. None of the phenotypic traits, essential to traditional generic concepts in Lobariaceae, i.e., the presence and type of pores in the lower cortex, defined a clade wherein all descendants exhibit the particular traits: pseudocyphellae and cyphellae no longer define a monophyletic Pseudocyphellaria and Sticta respectively. These pores have been shown to facilitate gas diffusion into the thallus[28,29,30] and may provide an adaptive advantage in temperate environments[31]. Phenotypic characters of the lichen association have been repeatedly shown to be poor phylogenetic predictors for the mycobiont[32,33,34], and the newly described genera, Crocodia, Parmostictina, Podostictina, and Yarrumia, may represent morphological/ecological chimeric forms between Pseudocyphellaria and Sticta

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