Character evolution of modern fly‐speck fungi and implications for interpreting thyriothecial fossils

Abstract

PREMISE OF THE STUDY:Fossils show that fly-speck fungi have been reproducing with small, black thyriothecia on leaf surfaces for ~250 million years. We analyze morphological characters of extant thyriothecial fungi to develop a phylogenetic framework for interpreting fossil taxa. METHODS:We placed 59 extant fly-speck fungi in a phylogeny of 320 Ascomycota using nuclear ribosomal large and small subunit sequences, including newly determined sequences from nine taxa. We reconstructed ancestral character states using BayesTraits and maximum likelihood after coding 11 morphological characters based on original observations and literature.We analyzed the relationships of three previously published Mesozoic fossils using parsimony and our morphological character matrix, constrained by the molecular phylogeny. KEY RESULTS: Thyriothecia evolved convergently in multiple lineages of superficial, leafinhabiting ascomycetes. The radiate and ostiolate scutellum organization is restricted to Dothideomycetes. Scutellum initiation by intercalary septation of a single hypha characterizes Asterinales and Asterotexiales, and initiation by coordinated growth of two or more adjacent hyphae characterizes Aulographaceae (order incertae sedis). Scutella in Microthyriales are initiated apically on a lateral hyphal branch. Patterns of hyphal branching in scutella contribute to distinguishing among orders. Parsimony resolves three fossil taxa as Dothideomycetes; one is further resolved as a member of a Microthyriales-Zeloasperisporiales clade within Dothideomycetes. CONCLUSIONS: This is the most comprehensive systematic study of thyriothecial fungi and their relatives to date. Parsimony analysis of the matrix of character states of modern taxa

Extending the fossil record for foliicolous Dothideomycetes: Bleximothyrium ostiolatum gen. et sp. nov., a unique fly‐speck fungus from the Lower Cretaceous of Virginia, USA

“…We hypothesize that combinations of morphological characters in fly‐speck fungi carry a phylogenetic signal that can be used to interpret fossil taxa (Le Renard et al, 2020a). By accumulating data on character combinations in individual fossils, we contribute to revealing broader patterns of radiations, extinctions, and change through time.…”

“…Fossil and extant fly‐speck fungi can be recognized from their thyriothecia, flat and circular sporocarps that are superficial on plant surfaces, in which a scutellum, a shield of pigmented hyphae, overlies spore producing tissue (Arnaud, 1918; Stevens and Manter, 1925; Germeraad, 1979; Wu et al, 2011; Guatimosim et al, 2015; Vishnu et al, 2017). Extant species consistently sporulate on leaf or twig cuticle, and ancestral state reconstructions show this habitat preference as evolving with or before the other distinguishing characters of their clades (Le Renard et al, 2020a). Cuticle has been available as a fungal habitat since the dawn of land plant evolution (Kerp, 2018; Guignard, 2019), more than 400 million years ago (Ma).…”

“…Extant fly‐speck fungi are now understood to be distributed across two classes and several orders of Ascomycota (Wu et al, 2011; Zeng et al, 2019; Le Renard et al, 2020a). Before DNA sequences became available, taxa with radiate scutella were classified in Microthyriales G.Arnaud, and taxa with non‐radiate scutella were placed in Hemisphaeriales Theiss.…”

“…Improving molecular phylogenies have led to new opportunities to evaluate the evolution of morphological characters across lineages of fly‐speck fungi (Le Renard et al, 2020a). Both the radiate and the non‐radiate forms are polyphyletic.…”

“…The radiate forms, originally placed in Microthyriales, are now distributed in different clades of a single class, Dothideomycetes O.E.Erikss. & Winka (Le Renard et al, 2020a). Combinations of characters of mycelium and of thyriothecial dehiscence mechanism (Wu et al, 2011; Hongsanan et al, 2015), and of ascus and ascospore morphology (Mapook et al, 2016a, b) help to characterize some of the newly recognized lineages (Le Renard et al, 2020a).…”