Introduction

The kingdom Fungi comprises an estimated 2 to 13 million extant species, many of which play important roles as constituents of continental ecosystems (Blackwell, 2011; Hawksworth and Lücking, 2017; Wu et al., 2019; Cheek et al., 2020). Fungi exhibit an extensive diversity of morphologies, reproductive strategies, and metabolic pathways; moreover, they enter into a broad spectrum of ecological relationships with other organisms, which may be dead or alive at the time of colonization (Willis, 2018). The ecological role of the common ancestor of the true Fungi remains elusive. However, early-diverging branches of the fungal stem lineage are parasites (Anderson et al., 2010).
Fossil fungi have been documented throughout the Phanerozoic (Taylor et al., 2015a), but fungal relationships with land plants and other fungi from the Lower Devonian, Carboniferous, Triassic, Cretaceous, and Cenozoic have attracted increased attention. The simple reason for this is the existence of exceptional rock or amber deposits from these periods of time that faithfully preserve numerous fungi together with their hosts, and thus provide direct insights into different levels of fungal interaction with other organisms in ancient ecosystems (Taylor and Krings, 2010; Taylor et al., 2015a, 2015b; Krings et al., 2017b, 2018; Halbwachs et al., 2021).
Documented fossil evidence of parasitic fungi in general is relatively rare, due primarily to the fact that, of all the potential levels of fungal interaction, parasitism is probably the most difficult to demonstrate based on fossils (Harper and Krings, 2021). Cherts, which are a dense microcrystalline or cryptocrystalline type of sedimentary rock deposits that may preserve organisms three-dimensionally and down to the finest cellular details, represent the most important sources of new evidence of fossil parasitic fungi. Coal balls, which typically are concretions of calcium carbonate, are another matrix that may yield exquisite fossils of parasitic fungi. A third copious source of information on parasitic fungi since the Cretaceous is fossilized plant resin called amber.
The fossil record of fungi as parasites was recently reviewed by Harper and Krings (2021). While these authors focus on the hosts, and describe fungal parasites of fossil land plants, algae, other fungi, and animals, here we use the (assumed) systematic affinities of the parasites as the guiding thread. This book chapter is aimed primarily at students and colleagues interested in having a concise overview of fossil parasitic representatives of the major lineages of fungi, and is complementary to the Harper and Krings (2021) review.

Fossils of parasitic fungi

Because not all branches of the fungal tree of life have a fossil record (Taylor et al., 2015a, 2015b; Krings et al., 2017b), and not all fungal lineages with a fossil record include parasites, the following compilation is limited to those lineages for which parasitism has been documented or suggested based on fossils, namely Chytridiomycota, zygomycetous fungi, Basidiomycota, and Ascomycota. Several fossil fungi that probably were parasites, but whose systematic affinities remain unresolved, are also included. Examples of fungal parasitism have been documented throughout the Phanerozoic (Harper and Krings, 2021). However, the Lower Devonian Rhynie chert of Scotland (~410 Ma), which is the oldest rock deposit containing comprehensive information on fungal life in a continental palaeoecosystem (Taylor et al., 2003, 2015a), and also several Mississippian and Pennsylvanian cherts (~331 Ma and ~304 Ma, respectively) from France and Early Pennsylvanian coal balls (~319 Ma) from England have been more systematically studied to date, and thus have yielded the largest number of examples. 

Chytridiomycota (chytrids)

Rhynie chert

The oldest fossil bona fide parasitic chytrids come from the Rhynie chert, and include holocarpic and eucarpic forms as parasites of land plants, charophytes, and other fungi (Kidston and Lang, 1921; Taylor et al., 1992b, 2015a; Krings et al., 2018). Three different forms have been identified as parasites of the charophyte Palaeonitella cranii (Fig. 1A; Taylor et al., 1992a). One of them, Milleromyces rhyniensis, is characterized by an endobiotic zoosporangium with a discharge tube extending out from the host cell wall. The other chytrids associated with P. cranii are Lyonomyces pyriformis and Krispiromyces discoides, which differ from one another in thallus morphology, but are comparable with several extant chytrid parasites of freshwater algae, including members of Entophlyctis and Phlyctochytrium. The host response in P. cranii is visible as a massive hypertrophy of cells, which grow to approximately five times the diameter of normal cells (Fig. 1B).
Rhizophydites matryoshkae is a monocentric chytrid from the Rhynie chert that parasitizes spores of the land plant Horneophyton lignieri (Fig. 1C; Krings et al., 2021). Zoosporangia are epibiotic, inoperculate, and possess 1–4 discharge papillae or short tubes. Several specimens comprise two or more successive generations of zoosporangia occurring one inside another (Fig. 1D), a feature that allows for a direct comparison with the extant genus Rhizophydium (Rhizophydiales).
Perhaps the most impressive parasitic chytrid from the Rhynie chert occurs on propagule clusters of unknown nature and affinity that are frequently encountered in microbial mats (Krings and Harper, 2019). Thalli consist of a robust, endobiotic or intramatrical rhizoidal system and an epibiotic sporangium, which is situated on the surface of the host cluster and arises from a prominent subsporangial inflation or apophysis (Fig. 1E). Some of the distal rhizoidal branches penetrate individual propagules and extend into their lumen. The rhizoid first forms a distally inflated, appressorium-like structure from which a narrow penetration peg is then pushed through the host wall.
Other monocentric and polycentric chytrids are colonizers and likely parasites of spores of arbuscular mycorrhizal fungi (Glomeromycota) in the Rhynie chert (Hass et al., 1994; Krings, 2022). Most are characterized by epibiotic zoosporangia and rhizoidal systems extending into the host spore lumen, others develop entirely within the spore lumen. An example of the former is Illmanomyces corniger, which consists of a zoosporangium with 4–5 conical discharge tubes (Fig. 1F) and a rhizoidal system that originates from a proximal protrusion on the sporangium (Krings and Taylor, 2014). Conversely, Globicultrix nugax is a polycentric thallus comprised of branched filaments and apophysate sporangia that are exclusively terminal (Fig. 1G; Krings et al., 2009b). The form has been compared with the extant genera Nowakowskiella and Cladochytrium (both Cladochytridiales). Finally, Brijax amictus develops largely within the wall of certain glomeromycotan acaulospores (Fig. 1H; Krings and Harper, 2020). Thalli consist of an inoperculate sporangium (zoosporangium or resting spore stage) located in the outer, ephemeral host spore wall component, and a rhizoidal system that extends into the inner, persistent spore wall. Briax amictus resembles certain present-day species of Phlyctochytrium (Chytridiales) and Rhizophydium (Rhizophydiales).
Hass et al. (1994), Krings and Harper (2018), and Krings (2022) describe penetration rhizoids of Rhynie chert mycoparasitic chytrids on glomeromycotan spores that extend into the host spore lumen and, once inside the lumen, become encased in a prominent, elongate-conical formation of newly synthesized spore wall material, termed a callosity (Fig. 1I). This host response is believed to prevent the rhizoid from extracting nutrients from the host. However, callosities in longitudinal section view reveal series of convex and concentric layers of varying thickness. This configuration indicates that the rhizoids continued to grow longer in spite of the presence of the callosity, and that the spores responded to the continued growth of the rhizoid by addition of new layers to the callosity. Krings and Harper (2018) regard callosity formation as evidence of biotrophy. Biotrophic relationships represent physiologically balanced systems, in which the parasite coexists with the host for an extended period of time and often forms specialized infection structures or host-parasite interfaces (Jeffries and Young, 1994; Jeffries, 1995). The arms race between the penetration rhizoid and the callosity can be viewed as a specialized host-parasite interface, in which the parasite is contained to a certain extent by the host, but is still able to grow and extract sufficient nutrients to provide for sporangium development and maturation. The consecutive layers comprising the callosities indicate that the host remained viable for an extended period of time while being parasitized.

Carboniferous, Mesozoic, and Cenozoic records

Fossil chytrids have also been reported from several Mississippian (Visean, ~331 Ma) and Late Pennsylvanian (~304 Ma) chert deposits in France. For example, Grilletia spherospermii and Oochytrium lepidodendri are two chytrid parasites of gymnosperms and arborescent lycophytes that have been described from these cherts more than 120 years ago (Renault and Bertrand, 1885; Renault, 1895, 1896). Additional evidence of chytrids has more recently been documented in (degrading) vascular plant tissues (xylem, periderm, cortical parenchyma, leaf mesophyll) and sporangia, as well as in various plant and fungal spores (Krings et al., 2007a, 2009a, 2009c, 2011b; Dotzler et al., 2011). Host responses possibly linked to chytrid infection occur in the form of callosities, some with a distinct penetration canal, in lycophyte xylem and periderm (Fig. 1J), as well as in glomeromycotan spores (Krings et al., 2009a).
Conspicuous spheroidal inclusions are sometimes present in gymnosperm pollen grains from the Upper Permian (~265 Ma) of India (Aggarwal et al., 2015). They occur in the corpus of the pollen grain, and have been interpreted as the remains of a pollen-colonizing organism, perhaps the endobiotic zoosporangia of a chytrid (Fig. 1K). Another putative endoparasitic chytrid, Synchtrium permicus, occurs in silicified plant remains from the Upper Permian of Antarctica (~255 Ma) (García Massini, 2007). The thallus is holocarpic and consists of thick-walled resting sporangia, thin-walled sporangia, and zoospores in different stages of development. The host cells are often hypertrophied. Morphology and development of the fossil suggest similarities with the extant genus Synchytrium (Chytridiales). Other fossils resembling Synchytrium have been reported from the roots of a Pennsylvanian calamite (~310 Ma) (Agashe and Tilak, 1970). They consist of mostly intercellular, oval to spheroidal sporangium-like structures containing numerous globular bodies.
The record of Mesozoic and Cenozoic chytrid parasites is exceedingly meagre. Pollen grains and spores obtained through palynological sampling sometimes contain structures that may represent chytrids. However, these structures do not normally receive attention because the focus of the research is directed at the pollen and spores, rather than their contents (Taylor et al., 2015a). A Mesozoic example of such an occurrence is Rhizophidites triassicus, a putative chytrid parasite of some Triassic spores that resembles the extant Globomyces pollinis-pini, which is a parasite of pine pollen (Daugherty, 1941). 

Zygomycetous fungi

Fossil evidence of zygomycetous fungi and their interactions with other organisms is rare. Not even the famous Rhynie chert has produced conclusive evidence of them (Krings et al., 2013a). The oldest bona fide fossils of zygomycetous fungi come from the Lower Pennsylvanian of England (~319 Ma) and occur in the form of several types of structurally preserved reproductive units interpreted as zygosporangia with attached gametangia (Krings and Taylor, 2012a, 2012b; Krings et al., 2013b). These fossils all have been discovered within the confines of plant parts, such as ovules and degraded wood. This is unusual since most modern zygomycetes produce zygospores aerially, on or in the soil, or on organic debris (Benny et al., 2001). As to whether the occurrence within plant parts reflects some life history strategy of Carboniferous zygomycetous fungi, perhaps plant parasitism, cannot be determined.
There are a few reports of putative parasitic zygomycetous fungi preserved in amber. For example, aseptate hyphae that resemble the assimilative hyphae of certain modern nematophagous zygomycetes occur in Miocene amber fossils of nematodes from Mexico (~20 Ma) (Fig. 1L; Jansson and Poinar, 1986). Another example is present in Cretaceous amber from Spain (~120 Ma) (Speranza et al., 2010), and occurs in the form of a thrip containing hyphae and reproductive structures similar to those seen in certain extant zygomycetes. Moreover, Poinar and Thomas (1982) describe an entomophthoralean fungus from a termite preserved in amber from the Miocene Dominican Republic (~18 Ma). The body of the animal is covered with a white mat composed of closely appressed (Fig. 1M), supposedly coenocytic hyphae. A layer of conidia lines the surface of the mycelial covering. Some of the conidia are budding and a number of smaller conidia (secondary conidia) are present in the amber close to the mycelial covering.