The Evolution of Life Modes in Stictidaceae, with Three Novel Taxa

Abstract

Ostropales sensu lato is a large group comprising both lichenized and non-lichenized fungi, with several lineages expressing optional lichenization where individuals of the same fungal species exhibit either saprotrophic or lichenized lifestyles depending on the substrate (bark or wood). Greatly variable phenotypic characteristics and large-scale phylogenies have led to frequent changes in the taxonomic circumscription of this order. Ostropales sensu lato is currently split into Graphidales, Gyalectales, Odontotrematales, Ostropales sensu stricto, and Thelenellales. Ostropales sensu stricto is now confined to the family Stictidaceae, which includes a large number of species that are poorly known, since they usually have small fruiting bodies that are rarely collected, and thus, their taxonomy remains partly unresolved. Here, we introduce a new genus Ostropomyces to accommodate a novel lineage related to Ostropa, which is composed of two new species, as well as a new species of Sphaeropezia, S. shangrilaensis. Maximum likelihood and Bayesian inference analyses of mitochondrial small subunit spacers (mtSSU), large subunit nuclear rDNA (LSU), and internal transcribed spacers (ITS) sequence data, together with phenotypic data documented by detailed morphological and anatomical analyses, support the taxonomic affinity of the new taxa in Stictidaceae. Ancestral character state analysis did not resolve the ancestral nutritional status of Stictidaceae with confidence using Bayes traits, but a saprotrophic ancestor was indicated as most likely in a Bayesian binary Markov Chain Monte Carlo sampling (MCMC) approach. Frequent switching in nutritional modes between lineages suggests that lifestyle transition played an important role in the evolution of this family.

Morphological and Phylogenetic Appraisal of Novel and Extant Taxa of Stictidaceae from Northern Thailand

“…The generic composition of Stictidaceae has been outlined by listing the genera name, but it lacks detailed annotations [ 4 , 5 , 6 , 7 ]. Thiyagaraja et al [ 20 ] introduced the novel genus Ostropomyces and accepted 32 genera following the previous outline. Molecular data are lacking for Biostictis , Conotremopsis , Delpontia , Dendroseptoria , Karstenia , Lillicoa , Nanostictis , Propoliopsis , Stictophacidium and Topelia.…”

“…Uniquely within Stictidaceae, Glomerobolus (in green area), a monotypic genus, reproduces via discharging a sticky propagule on fresh substrates rather than by producing sexual or asexual spores [ 19 , 22 ]. Molecular analyses have contributed substantially towards elucidating the natural classification of Stictidaceae [ 2 , 20 ]. Studies have attempted to ascertain phylogenetic relationships within and among species of Stictidaceae using different sequence datasets, such as individual SSU [ 12 ] and LSU [ 15 , 16 , 17 , 23 , 24 ] genes, as well as LSU-mtSSU-RPB2 [ 2 ] and LSU-ITS-mtSSU combined matrices [ 25 , 26 , 27 , 28 , 29 ].…”

“…Sexual morphs have been described for 26 genera in Stictidaceae. Members of this family typically develop apothecioid ascomata, except for Geisleria and Ostropomyces , where both possess perithecioid ascomata [ 18 , 20 ]. Most genera of Stictidaceae have cylindrical to clavate 8-spored asci.…”

“…Significant variation also exists among Stictidaceae genera regarding ascospore characteristics that might be informative in generic delimitation. The elongated clavate, long-cylindrical to filiform and multiseptate (>3-septate) ascospores can be observed in Absconditella [ 32 ], Cryptodiscus [ 13 , 33 ], Conotremopsis [ 34 ], Karstenia [ 13 ], Lillicoa [ 35 ], Nanostictis [ 13 ], Ostropa [ 13 ], Robergea [ 13 ], Acarosporina [ 13 ], Biostictis [ 35 ], Cyanodermella [ 15 ], Fitzroyomyce [ 36 , 37 ], Neostictis [ 36 ], Ostropomyces [ 20 ], Propoliopsis [ 13 ], Schizoxylon [ 13 ] and Stictis [ 13 ] ( Figure 1 ). The latter nine genera contain species whose ascospores can disarticulate into simple to septate part-spores or irregular fragments.…”

“…In most cases, their conidiomata are pycnidial, with the exception of Biostictis (with hyphomycetous sporulation structures) [ 35 ] and Dendroseptoria (with sporodochial fruiting bodies) [ 48 ]. Four modes of conidiogenesis have been observed in this family, including blastic-phialidic (i.e., Dendroseptoria [ 48 ], Neofitzroyomyces [ 23 ], Phacidiella [ 23 , 49 ], Fitzroyomyce [ 50 ], Cyanodermella [ 51 ] and Stictis [ 52 ]), blastic-sympodial (i.e., Eriospora [ 24 ], Biostictis [ 35 ] and Acarosporina [ 53 ]), blastic-retrogressive (i.e., Ostropomyces [ 20 ] and Schizoxylon [ 53 ]) and thallic-arthric (i.e., Hormodochis [ 17 ] and Schizoxylon [ 53 ]). Stictidaceae formed aseptate, one-celled to multiseptate, ellipsoidal to long cylindrical and occasionally tetraradiate conidia (see Figure 1 ).…”