The bulk of evidence of fossil parasitic Ascomycota comes from amber fossils and cuticle preparations of compressed leaves. However, the hitherto oldest putatively parasitic Ascomycota, Paleopyrenomycites devonicus, is from the Lower Devonian Rhynie chert, and is preserved in leaf-like enations, stems, and rhizomes of the early lycophyte Asteroxylon mackiei, where it produced ostiolate perithecia in substomatal chambers just beneath stomatal pores (Taylor et al., 1999, 2005). Necrotic areas in the host suggest that the fungus was a parasite. Hyphae and spores of another fungus, probably a mycoparasite, occur in several of the perithecia.

Fossils of parasitic fungi associated with animals primarily come from specimens enshrined in Cretaceous and Cenozoic amber. Perhaps the most spectacular example is a fungus described as Paleoophiocordyceps coccophagus, which was a parasite of scale insects and morphologically similar to present-day Ophiocordyceps (Sung et al., 2008). This fossil occurs in mid-Cretaceous Kachin amber (~100 Ma) from Myanmar in the form of synnemata emerging from the head of the insect (Fig. 2D). Another possible fungal parasite has recently been described from a Camponotus ant in Baltic amber (~45 Ma) as Allocordyceps baltica (Hypocreales: Clavicipitaceae) (Poinar and Maltier, 2021). The fungus is characterized by a stalked, cup-shaped ascoma with partially immersed perithecia that emerges from the rectum of the ant, two separate stromata with septate mycelium that emerge from the base of the neck and the abdomen of the ant, respectively, and free-standing putative perithecia bearing putative asci with multicellular ascospores. A third remarkable amber fossil preserving a fungus–animal interaction is a springtail (Collembola) covered in hyphae and conidiophores of an Aspergillus species that is also preserved in Eocene Baltic amber (Dörfelt and Schmidt, 2005). Most conidiophores extend directly from the host surface. The fungus may have penetrated and parasitized the living organism, and may have sporulated after the host had become entangled in liquid resin. The dominance of a single insecticolous fungus, together with the excellent preservation of the springtail, suggest a parasitic mode of life of the fungus (Fig. 2E).

A fossil member of the order Laboulbeniales, which are obligate ectoparasites (Haelewaters et al., 2021), is preserved on the thorax of a stalk-eyed fly in Bitterfeld amber (~24 Ma) from Germany (Rossi et al., 2005). The authors stated that the fungus is preserved in Baltic amber, but it is actually Bitterfeld amber (Perreau et al., 2021). This fossil was assigned to the extant genus Stigmatomyces, of which representatives are parasites of Diptera, and described as S. succinii. It is the oldest bona fide fossil representative of the class Laboulbeniomycetes (Fig. 2F, G). Another fossil attributed to the Laboulbeniales with confidence has recently been discovered in Miocene Dominican amber (~18 Ma) (Perreau et al., 2021). This fungus, Columnomyces electri, occurs on the leg of a leiodid beetle, and its discovery indicated that these beetles and their parasitic Laboulbeniales have coevolved at least since the Miocene (Fig. 2H, I).

A parasitic relationship involving an ascomycete has also been suggested for what has been interpreted as a Claviceps-like sclerotium, Palaeoclaviceps parasiticus, that occurs on a grass floret in Kachin amber (Fig. 2J; Poinar et al., 2015). The fossil is believed to demonstrate the existence of intricate interactions between Clavicipitaceae and the plant family Poaceae in the Cretaceous. Recently, Poinar (2020) reported on epiphyllous pycnidia, formally described as Palaeomycus epallelus, from an angiosperm leaf in Kachin amber, and suggested that, albeit no modern equivalents to these pycnidia are known, they are most similar to leaf spot-producing Coelomycetes (Fig. 2K). Finally, lichenicolous fungi of the genus Lichenostigma (Lichenostigmatales) occurring on the apothecial margin and crustose thallus of two lichen fossils preserved in Paleogene Baltic amber (~45 Ma) have been interpreted as parasites (Kaasalainen et al., 2019).

Examples of putative mycoparasitism and hypermycoparasitism have been reported from Kachin amber by Poinar and Buckley (2007). The gilled mushroom Palaeoagaracites antiquus is parasitized by an ascomycete, Mycetophagites atrebora. The mycelium of the parasite overgrows the pileus of P. antiquus and its hyphae also occur within the host tissue (Fig. 2L). A third organism involved in this interaction is Entropezites patricii, which appears to be a necrotrophic hyperparasite based on hyphae invading and apparently destroying the mycelium of M. atrebora (Fig. 2M). Another report of a fungal hyperparasite comes from the Eocene Princeton chert of Canada (Currah et al., 1998). Paleoserenomyces allenbyensis is an ascomycete preserved on permineralized leaves of the palm Uhlia allenbyensis. The fossil fungus shares certain features with extant Serenomyces (Phyllachorales), which also forms spots on palms (Hyde and Cannon, 1999). Present in some of the locules of P. allenbyensis are globose ascomata formally described as Cryptodidymosphaerites princetonensis (Melanommatales) that share morphological traits with Didymosphaeria, a genus of plant pathogens in Pleosporales.

The oldest fossil evidence in plant cuticles of a host response to the presence of a fungus comes from the Mississippian of Germany (~350 Ma) (Hübers et al., 2011). Pronounced cuticle rims bordering the margins of fungal thalli are interpreted as a host response suggestive of parasitism. A similar host response has been observed in a Jurassic Sphenobaiera (Ginkgophyta) leaf from China (~170 Ma) (Fig. 2N; Sun et al., 2015). Cuticle alterations probably linked to a fungal colonization have also been observed in Cenozoic angiosperm leaves from Australia (~30 Ma) (Tarran et al., 2016). Cuticular rims present on these leaves appear to have directed fungal hyphae away from the stomata, and thus away from the entry points into the leaves. Pteropus brachyphylli (Pleosporales) is a fossil ascomycete that occurs on leaves of a conifer from the Upper Cretaceous of Belgium (~67 Ma). Nearly all stomata of the host leaves are occupied by the fungus, suggesting that the association was parasitic rather than saprotrophic (van der Ham and Dortangs, 2005).

Compression fossils of Paleocene conifers of the Cupressaceae and Pinaceae from Russia (~60 Ma) show various types of damage, most of which were caused by Ascomycota (Maslova et al., 2021). Fungal remains obtained through cuticle preparations of the damaged areas include hyphae, chains of conidia, various types of fruiting bodies, and dispersed spores. The diversity of Ascomycota on these Paleocene conifers is consistent with previously obtained data on the existence of these plants in a temperate humid climate with a hot summer and without a dry season. There is astonishing diversity of fungal hyphae, fruiting bodies (e.g., thyriothecia, pycnidia), and hyphopodia, mostly of microthyriaceous fungi, also on Cenozoic angiosperm leaves. The vast majority of these remains have been obtained through maceration of compression fossils (e.g., Dilcher, 1965; Bannister et al., 2016). The nutritional modes of most of these fungi remain unknown; however, some authors have noted morphological similarities to present-day plant parasites and pathogens, such as Asterina, Vizella, and Trichothyrina (Taylor et al., 2015a).

Very often it is impossible to determine the systematic affinities of a parasitic fungus based on fossils. For instance, three morphologically different types of endophytic fungi occur in the prostrate axes of the Rhynie chert land plant Nothia aphylla (Krings et al., 2007b, 2007c). In spite of the exquisite preservation of the fungi, their affinities remain unclear. The association is nevertheless noteworthy because axes heavily infected by one of these fungi show a hypodermal zigzag line composed of secondarily thickened cell walls that appears to represent a specific host response effective in separating infected from uninfected tissues (Fig. 2O). Another fungus in N. aphylla triggers a host response in the form of encasement layers consisting of cell wall material that exclusively form around hyphae of this endophyte.

A truly enigmatic fossil from the Rhynie chert is Triskelia scotlandica, an acritarch-like structure with a prominent surface ornamentation. The form had been initially described as a green algal resting stage (Strullu-Derrien et al., 2021), but the subsequent discovery of specimens that occur in situ in prominent swellings of fungal hyphae provided strong evidence that it was not algal, but rather fungal in nature (Krings, 2021). Moreover, specimens with a discharge tube suggest that T. scotlandica may be a zoosporangium or resting spore stage of an endoparasite (Fig. 2P), perhaps with affinities to holocarpic Oomycota (e.g., Olpidiopsis), Cryptomycota (e.g., Rozella), or zoosporic Fungi (e.g., Olpidium), in which case the hyphal swellings would be either dilatations resulting from the expansion of the parasite inside, or a host response (hypertrophy).

A geologically younger, presumably parasitic fungus of unknown affinity is Cashhickia acuminata, which is preserved in permineralized calamite roots from the Upper Pennsylvanian of central France (~304 Ma) (Taylor et al., 2012). Infected roots contain intracellular hyphae in the outer cortex that arise from a meshwork-like mycelium extending between cortical cells. All intracellular hyphae are oriented towards the root centre. Within the cortical cells are host responses in the form of callosities that indicate the roots were alive at the time of infection (Fig. 2Q). Fossils similar to C. acuminata have been described in roots from the Triassic of the Svalbard archipelago by McLoughlin and Strullu-Derrien (2016). Other evidence of fungal parasitism in Pennsylvanian plants occurs in a Lasiostrobus polysaccii cone from Illinois, USA (~310 Ma) (Stubblefield et al., 1984). On the inner surface of cortical cells containing fungal hyphae are peculiar swellings that appear to represent wall appositions produced by the host in response to the infection.

Septate fungal hyphae present in silicified Agathoxylon (Araucariaceae) wood from the Upper Cretaceous (~84 Ma) of South Africa have been compared with blue-stain fungi colonizing the wood of present-day Pinus strobus (Strullu-Derrien et al., 2022). They represent the first documented evidence of these wood-colonizing Ascomycota in the geological record. Structures interpreted as fungal mycelia of uncertain affinity have also been found in sections of dinosaur egg shells from the Upper Cretaceous (~80 Ma) of central China (Gong et al., 2008). Based on fungal morphology and the areas in the shells in which the fungi occur, it has been hypothesized that the fungi were parasitic and invaded the eggs before they became lithified.

Fungi today master very different levels of interaction with various other organisms. They form lichens, enter into mutualistic relationships with plants and animals, occur as endophytes in virtually all land plants, and negatively affect the functions of other microorganisms, plants, animals, and even humans as parasites and pathogens (Kaishian et al., 2022). Fungi probably had similar roles in the geologic past. Documenting these roles based on fossils is a challenging task, foremost because of the low preservation potential of most fungal life cycle stages, and because the majority of fungal fossils occur dispersed and are fragmented (Taylor et al., 2015a). It is clear from the examples of fossil fungal parasitism presented in the sections above that the key to understanding fungi as constituents of past ecosystems is the extraordinary preservation found in certain rock deposits. While the Rhynie chert of Scotland is perhaps the prime illustration of this, there are other fossil ecosystems that have been preserved in a similar manner, but to date have received less attention (e.g., García Massini et al., 2012; Klymiuk et al., 2012; Harper et al., 2016). As more information is gathered on the fungi preserved in these deposits, and as further rock deposits containing well preserved fungi are unearthed, additional examples of fungal parasitic interactions will be discovered and described. This will provide increasing opportunities to relate fossils to extant analogues to better understand the past diversity, evolutionary history, and past ecological functions of parasitic fungi.

C.L. is supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB26000000), the Second Tibetan Plateau Scientific Expedition and Research (2019QZKK0706), and the National Natural Science Foundation of China (42125201, 41688103). D.H. was supported by the Research Foundation – Flanders (FWO Junior Postdoctoral Fellowship 1206620N). M.K.’s research on fossil fungi received funding from the U.S. National Science Foundation (EAR-0542170, EAR-0949947, and DEB-1441604–S1696A-A), the Alexander von Humboldt Foundation (V-3.FLF-DEU/1064359), and the Deutsche Forschungsgemeinschaft (KE584/13-2, KR2125/5-1). M.K. thanks Hans Kerp and Hagen Hass (both Münster, Germany), Nora Dotzler (Munich, Germany), Jean Galtier (Montpellier, France), Carla J. Harper (Dublin, Irleand), Christopher Walker (Gloucester, UK), Edith L. Taylor (Lawrence, KS, USA) and Thomas N. Taylor (†) for fruitful collaboration over many years. The chapter benefited greatly from constructive comments and suggestions by Alexander R. Schmidt (Göttingen, Germany).