The enigma: . Already during the 19th century, several meters high were detected. Initially, they were interpreted as archaic , then as , rolled liverworts, or giant (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 Hans Halbwachs ABSTRACT of fossils; what evidence we have is fungal on biotic and abiotic Fungal evolution goes back for at least preserved geological strata or . environmental circumstances, which two billion years. From flagellate marine Through molecular analysis methods sheds some light on the consequences of to terrestrial Asco–and (examining the “molecular clock”), the present degradation of . , fungal –and the fungal pathway through ’s the radiation of those –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- symbiotic) innovations. The 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. 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 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. (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 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 includes used to calibrate the approximately 500 species, but 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 . 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 largely unknown. Science is not from 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: ? or to the issue of fossilized fungi in more Diversity and ? (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 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 , 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 () (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 (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 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 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 Figure 1. Cladogram illustrating radiation, beginning with the production above the substrate surface, (depicted as root of the 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 Ma General effects Effects on fungi

Ordovician/ ~444 85% of all species died out, Unknown mainly marine taxa.

Devonian ~360 75% of all species died Due to the decreasing oxygen content of seas, possibly out, mainly reef-building selective pressure to become terrestrial occurred. organisms.

Permian/ 260–252 96% marine and 65% of Especially plants were affected. A rapid rise of fungal terrestrial species perished, species because of the enormous masses of plant remains probably because of a (white and brown rot) (Steiner et al., 2003). In the dramatic rise of temperature aftermath, fungal diversity and abundance could have between 5° and 10°C. collapsed again due to the depletion of the substrate. Beimforde et al. (2014) suggested that the ecological diversity in all ascomycete lineages was responsible for the survival of at least some taxa of each group, despite global crises.

Triassic/ ~210 Probably triggered by massive Changes in the prevailing modes of primary production volcanism, ca. 80% of all could have compromised fungal diversity (Pieńkowski et species perished. al., 2011).

Cretaceous/ ~66 Probably triggered by a Probably only temporary effects on fungi (Sweet and Paleogene colossal meteorite impaction, Braman, 2001). ca. 75% of all organisms died out (!).

Table 2. The “Five Big Mass Extinctions” (Boenigk et al., 2015). radiation (Table 2). However, it may not have been that simple. The “Big Five” may have led to drastic transformations of the environment and species spectra, at least regarding plants (McElwain and Punyasena, 2007). It also should have affected fungi, which depend on plants in multifaceted ways. Such allegedly catastrophic events may lead to the creation of new environmental niches, among other things, and explosive species diversifications. One starting point could have been the last extinction episode ca. 60 MYA. It is apparent that mushrooms Figure 2. The strongly ornamented , Hebelomataceae and made a jump ahead, as shown in Fig. have significantly higher diversification rates than, e.g., . Sources: 1. It appears that massive speciation Ryberg and Matheny (2011), spore images Knudsen and Vesterholt (2012), courtesy events are a result of specific genetically Henning Knudsen. induced morphological innovations that are connected to the dispersal fitness dispersal (Fig. 2). Spore ornamentation entailed differing DNA codes (“Mating of fungi (Lomolino et al., 2006). In the could imply advantages in dispersal System”), which essentially served to meantime, the Big Five are under dispute; by invertebrates such as collembola, avoid detrimental inbreeding (Box it is argued that fossil records have been because may better get into 2). Which key innovations or their misinterpreted (Racki, 2019). the soil and close to host roots with combinations led to notable speciation In any case, another radiation such vectors (Halbwachs et al., 2015; boosts is still largely unknown. Also, event refers to the conspicuously Halbwachs and Bässler, 2015; Calhim et not only the already-mentioned lineages multiple diversifications of some al., 2018). Whether such a connection is were subject to intense radiations. ectomycorrhizal groups, which it real, remains speculative to date. Some other macromycetes show similar seems have developed pronounced Now, another key innovation in the dynamics (Fig. 3). Marasmius is such a ornamentation as key innovations in evolution of fungi: sex! Initially, it only candidate with high diversity, despite 18 FUNGI Volume 13:2 Summer 2020 fungal inclusions in amber, taxonomic attributes are better discerned. Still, Box 2: Mating systems. even supposedly well-preserved Fungi being eukaryotes (having cells with a nucleus) are generally not morphological traits of fungi in amber able to reproduce under the exchange of (recombination) by fusing may lead down a wrong interpretive hyphae, and their cell nuclei (karyogamy) followed by nuclear division. track: a mushroom-shaped specimen This process shuffles the genetic attributes of two individuals resulting in was classified as Palaeocybe striata by an offspring that recombines the characteristics of the parents. It creates Dörfelt and Striebich (2000), which a genetic diversity that better enables fungi to adapt, e.g., to changing Schmidt and Dörfelt (2007) several years environmental conditions. Therefore, an exchange of identical or similar later identified as an extinct member genetic information would be of little use (Fraser and Heitman, 2004). To of Matoniaceae, a dwarf . However, avoid this, mating systems ensure that only recombination can take place such errors do not negate the work of if allowed by specific markers (see Moore et al., 2011). Precursors of scientists nor the value of fungal fossils, such a mechanism are already present in zygomycetes (Dyer, 2008), which especially in the case of higher fungi putatively originated during the Precambrian (Taylor et al., 2015). found in amber (Poinar Jr, 2016) (Box 3). The state of preservation is mostly better than of fossils from sediments and rocks, even if they are often not easily an inconspicuous morphology and a or the evolvability of fungi. investigated by optical means (Penney saprobic lifestyle. and Green, 2010). Additional approaches to explaining Fossil witnesses differences in species numbers relate to A great deal of what we know of the ecological and regional factors (Rabosky, fungal past, we owe to fossils even if, Since the (ca. 530 MYA, 2009). Moreover, some chromosomal due to their ephemeral nature, only a Prieto and Wedin, 2013) sac fungi have mechanisms, e.g., transposons (“jumping few have persisted (Taylor et al., 2015). become a substantial part of the present genes,” which may accelerate evolution) However, such fossils often have the fungal flora with 64,000 described (Bromham, 2016), may be relevant disadvantage of being preserved merely species (Kirk et al., 2011). Unequivocal to help explain the erratic speciation as imprints, which only allow limited records from earlier periods are patterns in fungi. All this diversity interpretations. Therefore, errors are rather meager and of little informative demands research concerning, e.g., the preprogrammed, even for experienced value. Only the already mentioned effects of morphological traits on the paleontologists and mycologists. Due find in provides definite fungal reproductive and dispersal fitness to the three-dimensional nature of proof (Fig. 4a). Another example is an

Figure 3. Diversity patterns of some agaricomycete lineages (tree based on Matheny et al., 2006; Miller et al., 2006; Matheny et al., 2007). The approximate species numbers in brackets behind the family names have been taken from Kirk et al. (2011). Green symbols denote wholly or partially ectotrophic families, grey denotes saprobic groups.

Summer 2020 FUNGI Volume 13:2 19 in Dominican amber (Fig. 4b). Basidiomycota The Basidiomycota are ca. 60M years older than the Ascomycota (Taylor and Berbee, 2006). By 2011, almost 32,000 species had been described (Kirk et al., 2011). The determinants of Basidiomycota, being more species-poor than Ascomycota, are multifaceted. For one, the evolutionary pace (speciation rate) is about 20% higher in ascomycetes, in which the species-rich sordariomycetes evolve particularly fast (Wang et al., 2010). Conspicuously, ascomycetes possess, on average, a 20% larger genome than basidiomycetes, without any clues as to why (Mohanta and Bae, 2015). For whatever reason, some organismal groups with large Figure 4. a) Longitudinal section of a perithecium of Paleopyrenomycetes devonicus genomes do have a higher speciation Taylor, Hass, Kerp, Krings et Hanlin from Rhynie Chert (ca. 400 MYA). Source: Taylor rate (e.g., some fish, Kraaijeveld, 2010), et al. (1999), Springer license No. 4558171315501; bar 50 µm. b) Conidia of an and this is perhaps the case with the Aspergillus (Lower Miocene, ca. 17.5 MYA). Source: Thomas and Poinar Jr (1988), ascomycetes. In the end, speciation courtesy George Poinar; bar 100 µm. rates cannot be explained by a single 20 FUNGI Volume 13:2 Summer 2020 Figure 5. a and b) Ascospores in a plant fragment (Sumatra, Miocene ~23 MYA), 6.5x13 µm and 10x18 µm. c) (Mexico, ~16 MYA), 13x35 µm. d) Ascospores cf. Peziza sp. (Mexico, ~16 Ma), 10x20.5 µm. All images by the author.

Some micro-fossils have been isolated by the solvent method and these specimens can be attributed to basidiomycetes (Halbwachs, 2019a) (Fig. 9). One can be sure that more finds of this kind will appear, which may fill gaps in the fossil record. Parasites and symbioses Fungal endophytes have apparently played a crucial role in the conquest of land, with a fuzzy passage from parasites to mutualists (see Box 4) (Krings et al., 2012). Arbuscular hyphal structures from strata of the German Lower are one example (Fig. 10). Associations with animals are likewise rather old. In the Burgsvik Sandstone (Gotland, Sweden, Upper Silurian ~425 MYA) Sherwood-Pike and Gray (1985) found coproliths (fossil excrements) of soil arthropods (springtails, mites or millipedes) associated with masses of hyphae and spores of ascomycetes (Fig. 11). In this case, the evidence points to fungi as a nutrient source. It should also be noted that most of the “mosquitos” found in amber are fungus gnats (Ross, 2010), which points to a rich fungal flora in humid-temperate to tropical amber forests at that time. In early terrestrial Earth history, symbiotic associations ( to , see Box 4) are known first to occur together with plants, a condition which may have been required in for fungi to colonize land (Selosse and Strullu-Derrien, 2015). In the process, lichens took an exceptional position because of their extreme adaptability (Taylor et Figure 6. Gondwanagaricites magnificus from Chapada do Araripe, al., 2015). They count as forebears of fundamental Ceará, Brazil. Gill remains are identifiable on the left upper part. ascomycete groups as Aspergillus and Penicillium Source: Heads et al. (2017), License: Attribution 4.0 International (CC (Lutzoni et al., 2001). The alliance between fungi, BY 4.0). Link: creativecommons.org/licenses/by/4.0/deed.de. cyanobacteria, and also algae is an evidently successful factor. The interrelations and causalities are too complex and, symbiosis because it arose independently around 30 therefore, require more intense research, especially at the molecular times (!) during Earth’s history (Lücking and Nelsen, level. Currently, the oldest known fossil of a macro-basidiomycete 2018). Particularly intense radiations began by the originates from the Cretaceous (ca. 115 MYA). It is a gilled Paleogene ca. 50 MYA (Kettunen et al., 2017), as is mushroom, described as Gondwanagaricites magnificus, belonging evidenced from Bitterfeld amber (Fig. 12). to the Agaricales (Heads et al., 2017). The fossil exhibits the typical However, parasitic associations, e.g., between fungal architecture of a mushroom (Fig. 6). pests and plants, can cause an accelerated evolution. So far, the oldest known hyphae of a white rot fungus with clamp Parasitic associations induce the syndrome of the connections were described from the Lower Cambrian (Fig. 7). so-called “Red Queen,” a character in Lewis Carroll’s Summer 2020 FUNGI Volume 13:2 21 parable Alice Through the Looking Glass, who was forced to run ever faster to keep in place. Parasites trigger defense responses in the host, which in turn provoke adaptations by the parasite to breach the host’s improved armament. Thus, an evolutionary chain reaction is initiated that leads to accelerated speciation (Van Valen, 1977). A further pivotal development, which began ca. 200 MYA, was the multiple emergences of ectotrophic associations between woody plants and asco- or basidiomycetes. A spectacular example has been detected in Indian amber (“Cambay amber”) (Fig. 13). The multiple emergences of a mutualistic lifestyle during the evolution of fungi (primarily mycorrhizae) entail new ecological opportunities and hence lead to significant radiations (Lutzoni and Pagel, 1997; Hoysted et al., 2018). Impulses What does the neverending story of fungi teach us? There were conspicuous speciation bursts, a phenomenon in line with the theory of the “” of Eldredge and Gould (1972), who postulated that evolution occurs in erratic jumps. The erratic radiations of fungi were mainly sparked off by: • Symbiotic associations, primarily with plants as endophytes (Krings et al., 2012). • The emergence of the lichens (Lücking and Nelsen, 2018). • Mycorrhizae were exceedingly innovative and successful in shaping and boosting resilience of ecosystems Figure 7. Hyphae of a ca. 135M old basidiomycete with clamp connections. Source: (van der Heijden et al., 2015). (Tian et al., 2018), courtesy Ning Tian; bar 10 µm. • The emergence of mushrooms in the Agaricomycotina, which led to higher reproductive and dispersal fitness (Varga et al., 2019). This interpretation may well be too simplistic because this radiation involved a variety of morphological traits and combinations (Zmitrovich and Wasser, 2011). • (Partial) extinctions like those documented towards the end of the Cretaceous, during which two-thirds of all life perished. Figure 8. Basidiomycete fossilized in amber. a) baltica (Baltic, Eocene ~36 MYA); b) Palaeoagaracites antiquus (Myanmar, Upper Cretaceous ~100 MYA); c) What's next? Evolution is not a Coprinites dominicana (Dominican Republic, Miocene ~18 MYA). Source: Poinar Jr directional force that only proceeds (2016), all images courtesy George Poinar; bars 1 mm. towards “improvement.” Evolution is a tinkerer (Jacob, 1977) that works with 22 FUNGI Volume 13:2 Summer 2020 Figure 9. Micro-fossils of basidiomycetes isolated from amber. a) cf. (Baltic, Eocene ~36 MMY); b) cf. sensu lato (Baltic, Eocene ~36 MYA); c) with clamp connection (Sumatra, Miocene ~23 MYA); bars 10 µm. All images by the author.

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