Multiple historical processes obscure phylogenetic relationships in a taxonomically difficult group (Lobariaceae, Ascomycota)

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.

Genome-scale data reveal the role of hybridization in lichen-forming fungi

“…Our results support the need for considering reticulate phylogenies when investigating species boundaries and evolutionary history, even in well-supported topologies inferred from genome-scale data. Similarly, while the role of hybridization and recombination has long been considered in diversification of lichen-forming fungi 33,[41][42][43] , our results provide important impetus for explicitly considering hybridization/introgression in process of speciation in symbiotic fungi and their potential role in generating novel phenotypes and introducing reproductive barriers.…”

“…With a poor fossil record 37,38 and potentially unreliable phenotype-based classification 39 , options for elucidating the evolutionary history of lichen-forming fungi was challenging prior to the development of modern molecular tools. Potential evidence of hybridization has been encountered in a number of lichen-forming fungal lineages 33,[40][41][42][43] . However, genome-scale datasets have not yet been used to explicitly infer the role of hybridization on the process of speciation lichen-forming fungi.Characterizing gene flow is further complicated by a diverse range of reproductive strategies used by lichen-forming fungi 44,45 .…”

Elucidating species richness in lichen fungi: The genusSticta(Ascomycota: Peltigeraceae) in Puerto Rico

“…Phylogenetic relationships within this group were recently assessed by Widhelm & al. (2019) using a target enrichment approach of 400 single‐copy nuclear genes. Although conflicting topological patterns among data types and phylogeny reconstruction methods used were observed, Sticta was most often recovered as sister to Yarrumia D.J.Galloway, a recently segregated genus from Pseudocyphellaria (Galloway, 2015) not included in Moncada & al.…”

“…Complex historical processes might also underlie some of these conflicts, as has been recently proposed by Widhelm & al. (2019). These could potentially confound phylogenetic reconstructions and result in clades with short branches and poor support, such as the one containing Clades I, II, III and V in Fig.…”

“…s.l. (Moncada & al., 2013b; Widhelm & al., 2019), excluding taxa recently segregated to the genus Lobaria (Schreb.) Hoffm.—that is, L. anomala (Brodo & Ahti) T.Sprib.…”