Accelerated diversifications in three diverse families of morphologically complex lichen-forming fungi link to major historical events

Jen-Pan Huang,Ekaphan Kraichak,H Thorsten Lumbsch,Steven D Leavitt,Matthew P Nelsen

doi:10.1038/s41598-019-44881-1

Abstract

Historical mass extinction events had major impacts on biodiversity patterns. The most recent and intensively studied event is the Cretaceous – Paleogene (K-Pg) boundary (ca. 66 million years ago [MYA]). However, the factors that may have impacted diversification dynamics vary across lineages. We investigated the macroevolutionary dynamics with a specific focus on the impact of major historical events such as the K-Pg mass extinction event on two major subclasses – Lecanoromycetidae and Ostropomycetidae – of lichen-forming fungi and tested whether variation in the rate of diversification can be associated with the evolution of a specific trait state - macrolichen. Our results reveal accelerated diversification events in three families of morphologically complex lichen-forming fungi – Cladoniaceae, Parmeliaceae, and Peltigeraceae – which are from the subclass Lecanoromycetidae and mostly composed of macrolichens, those that form three dimensional structures. Our RTT plot result for the subclass Lecanoromycetidae also reveals accelerated diversification. Changes in diversification rates occurred around the transition between Mesozoic and Cenozoic eras and was likely related to the K-Pg mass extinction event. The phylogenetic positions for rate increases estimated based on marginal shift probability are, however, scattered from 100 to 40 MYA preventing us from making explicit inference. Although we reveal that the phenotypic state of macrolichens is associated with a higher diversification rate than microlichens, we also show that the evolution of macrolichens predated the K-Pg event. Furthermore, the association between macrolichens and increased diversification is not universal and can be explained, in part, by phylogenetic relatedness. By investigating the macroevolutionary dynamics of lichen-forming fungi our study provides a new empirical system suitable to test the effect of major historical event on shaping biodiversity patterns and to investigate why changes in biodiversity patterns are not in concordance across clades. Our results imply that multiple historical events during the transition from Mesozoic to Cenozoic eras, including the K-Pg mass extinction event, impacted the evolutionary dynamics in lichen-forming fungi. However, future studies focusing on individual lichen-forming fungal families are required to ascertain whether diversification rates are associated with growth form and certain geological events.

Highlights

The five mass extinctions in earth’s history had major impacts on biodiversity, reshaping entire ecosystems and resulting in dramatic changes in the diversity of major clades[1,2,3,4]
The study of macroevolutionary dynamics has been revolutionized by molecular phylogenetic and comparative methods, these methods assume that the studies have complete taxon sampling or have been adjusted for missing samples
We only reveal that their effect on the variation of macroevolutionary dynamics do not result in statistically detectable differences using currently available data

Summary

Introduction

The five mass extinctions in earth’s history had major impacts on biodiversity, reshaping entire ecosystems and resulting in dramatic changes in the diversity of major clades[1,2,3,4]. Recent comparative phylogenetic studies have indicated that the K-Pg mass extinction event may have facilitated the subsequent rapid diversifications in modern day birds, their lice, and frogs[12,13,14] These specific shifts have been proposed to facilitate the radiation of major clades of mammals, such as rodents[15], which account for approximately 42% of extant mammalian diversity[16], and of plant clades with duplicated genomes[17]. We examine how major historical events and different diversification rates associated with a trait have shaped the diversity of lichen-forming fungi. Within a comparative phylogenetic context, we studied the association between the evolution of different trait states and major historical events and tested whether this putative evolutionary innovation may have accelerated diversification in lichen-forming fungi. Our results provide a diversification history of lichen-forming fungi in general and provide specific novel insights into how major historical events, such as the K-Pg mass extinction, might (or might not) impact diversification of mutualistic fungi

Objectives

Methods

Results

Conclusion