The Devonian enigma: Prototaxites. Already during the 19th century, fossils several meters high were detected. Initially, they were interpreted as archaic plants, then as algae, rolled liverworts, or giant lichens (Moore et al., 2011). Recently, evidence has been mounting that they may have been ascomycetes, possibly lichenized (Retallack and Landing, 2014; Honegger et al., 2017). More information on Prototaxites (and much more) can be found in www.davidmoore.org.uk. Painting image courtesy Geoffrey Kibby (British Mycological Society). Fungi in the rear mirror A brief history of the fungi during the last two billion years Hans Halbwachs ABSTRACT of fossils; what evidence we have is fungal evolution on biotic and abiotic Fungal evolution goes back for at least preserved geological strata or amber. environmental circumstances, which two billion years. From flagellate marine Through molecular analysis methods sheds some light on the consequences of Chytridiomycota to terrestrial Asco–and (examining the “molecular clock”), the present degradation of nature. Basidiomycota, fungal speciation–and the fungal pathway through Earth’s the radiation of those species–occurred history can be amended and ancestral Keywords: Basidiomycetes, ascomycetes, through multiple steps that were mainly relationships elucidated. In the following fossils, amber, evolution, symbiosis, triggered by key morphological (often historical review, important, history- Agaricomycotina symbiotic) innovations. The fossil record illuminating fossils are depicted and put Author’s address: Hans Halbwachs, does document such evolutionary steps, into evolutionary context. It also Danziger Str. 20, 63916 Amorbach, albeit incompletely due to the scarcity describes the delicate dependencies of Germany, E-mail: [email protected] 14 FUNGI Volume 13:2 Summer 2020 The mysteries of fungal evolution The sheer magnitude of extant fungal Box 1: How is the molecular clock ticking? diversity, with probably more than 2.2 Each organism is subject to alterations of its DNA and proteins. Mutations also million species, is baffling (Hawksworth occur in neutral sequences, which do not affect the phenotype, i.e., do not and Lücking, 2017). This number underlie selective pressure. Given that the mutation rate of such neutral indicates that fungi are an old kingdom, sequences remains the same through time, they can be used to estimate the point perhaps one of the oldest among when two species diverged in the course of the evolution. eukaryotes (organisms with a distinct Each dash nucleus in their cells). The magic of the symbolizes a fungal kingdom’s diversity becomes mutation (intermittent particularly visible, specifically, in the Agaricales branches are “higher” fungi, with its enormous but omitted here). unevenly distributed phylogenetic and Common Fossils with known morphological diversity. For example, ancestor geological age are why does genus Marasmius includes used to calibrate the approximately 500 species, but Agrocybe Boletales calculated time only 35 (Kirk et al., 2011)? spans. Source: Apart from the question of how Donoghue and fungi emerged, the observed diversity Smith (2003). patterns beg for explanations. In other words, what were (and are) the drivers of If it only were that simple! Sadly, the mutation rates are not so constant as initially assumed (Bromham, 2016). For instance, Beimforde et al. (2014) showed speciation and associated phylogenetic an uncertainty of 100 million years on the divergence of Helvella and Gyromitra peculiarities? This review aims to towards the end of the Cretaceous. Finally, one should realize that cladistic present a synopsis of the evolution of methods are based on statistics, which are inevitably accompanied by fungi as well as to cast a little light onto uncertainties (Nagy et al., 2012). some darker corners of fungal phylogeny. How it (perhaps) began To be clear right from the beginning, Where did these authors get their speciation surges (“radiations”), rather how the first fungi evolved remains data? First of all, fossils are recovered uneventful periods, and extinctions largely unknown. Science is not from sediments and other rocks and, (Boenigk et al., 2015). at all sure what appeared first on notably, from amber; I will come back the evolutionary scene: plant? or to the issue of fossilized fungi in more Diversity and extinction fungus? (Hedges et al., 2006). Or if detail later on. The second and most As I have noted, the history of the both at the same time? A visionary important source of data are molecular Earth is a turbulent one. Above all, British mycologist even assumed that clocks. Despite some uncertainties volcanic and tectonic forces shaped LUCA (the “Last Universal Common (see Box 1), the method has become a mosaic of land and sea. The period Ancestor“), the forebear of all eukaryotic indispensable for elucidating the when life emerged was particularly living things, was a fungus (Moore, evolutionary pathway of fungi. uncomfortable for sure because of 2013). Widely accepted now is the The more one goes back in time, the frequent meteorite impacts (Boenigk view that ancestral plants and fungi more inherently dubious the inferences, et al., 2015). What we would consider developed in the primeval seas of the because fossils for calibrating the extreme environmental upheaval Precambrian, namely algae and flagellate molecular clock are seldom available. may have contributed to the lack fungi (Chytridiomycota sensu lato) One should not be surprised that the of observable specimens along the (Hedges et al., 2006). The current oldest suggested divergence time between evolutionary path that led to the advent fungal fossil is probably 2.4 billion years basidio- and ascomycetes varies between of fungi. The further evolution can be old (Paleoproterozoic) (Bengtson et al., 900 million (Hedges et al., 2006) and 650 inferred with the help of fossils and the 2017). The first fungal steps on land million years (Tedersoo et al., 2018). molecular clock. It should be noted that took place circa one billion years ago, Back to conquering land. We had during this process, fungi and plants likely before plants (Hedges et al., 2006). unruly times in those days towards the are usually found in association with The still-quite-hostile terrestrial habitat end of the Ordovician (ca. 450 MYA). one another shortly after the “conquest” (little oxygen, intense UV radiation) Wildly oscillating sea levels, high carbon of land (Boenigk et al., 2015). The only allowed an expansion of biocrusts, dioxide concentrations, and fierce somewhat erratic fungal paleohistory is which were composed of heterotrophic volcanic activities (Edwards et al., 2015), presented in Table 1. bacteria and cyanobacteria (Taylor et paradoxically created a concoction The diversity graph (based on the al., 2015). These biocrusts, together with of circumstances that accelerated currently described taxa from amber, see first terrestrial fungi, could have formed speciation through selective forces and Halbwachs, 2019b) in Table 1 depicts the a mutualistic-lifestyle organism similar geographical isolation (Levin, 2004; evolutionary steps only in a flashlight to lichens (Yuan et al., 2005; Strullu- Mayhew, 2006; Schluter, 2017). The fashion. Still, the key events become Derrien et al., 2018). onward march of the fungi is paved with clear. Red bullets flag particularly Summer 2020 FUNGI Volume 13:2 15 16 FUNGI Volume 13:2 Summer 2020 o Table 1. Compilation of fungal evolution in the course of Earth’s history based on innovative developments which, for the fossil and molecular data. In the last column, the accompanying dynamics of fungi most part, resulted in intense radiations. (blue) and plant (green) evolution is schematically depicted. Red arrows denote I want to highlight the first fungus-plant mass extinctions. The color code and the classification follow the International symbioses because they likely triggered Commission on Stratigraphy (www.stratigraphy.org). Sources: Berbee and Taylor co-evolution and thus contributed (2001); Wellman (2003); Wikström et al. (2003); Binder and Hibbett (2006); Matheny to the acceleration of adaptations to et al. (2006); Miller et al. (2006); (2008); Soltis et al. (2008); Bidartondo et al. (2011); changing environmental conditions Krings et al. (2011); Ryberg and Matheny (2011); Bonito et al. (2013); Boenigk et al. (Thompson, 2017). In the same way, the (2015); Taylor et al. (2015); Bengtson et al. (2017); Lutzoni et al. (2018); Seyfullah et emergence of mushrooms ca. 180 MYA al. (2018); Strullu-Derrien et al. (2018); Loron et al. (2019); Varga et al. (2019). sparked explosive radiation of species, possibly due to the lifting of spore Figure 1. Cladogram illustrating mushroom radiation, beginning with the production above the substrate surface, Carboniferous (depicted as root of the phylogenetic tree in the center) (modified making spore dispersal significantly after Varga et al., 2019). The explosive split-ups of the lineages within the more effective (Varga et al., 2019). The Agaricomycotina mainly took place at the beginning of the Paleogene (ca. 60 MYA). staggering diversification becomes The insert in the center shows the diversification rates as hues (the warmer, the evident with a cladogram (Fig. 1). higher). License: Attribution 4.0 International It seems rather remarkable that (CC BY 4.0), Link: creativecommons. mass extinctions did not leave org/licenses/by/4.0/deed.de. visible traces in fungal Summer 2020 FUNGI Volume 13:2 17 Period