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Britt A. Bunyard Onto the Scene Around 245 MYA Figure 1. Palaeoagaracites antiquus from Burmese amber, 100 MYA. This is the oldest-known fossilized mushroom. Photo courtesy G. Poinar. Britt A. Bunyard onto the scene around 245 MYA. Much of what we know of extinct ow old are the oldest fungi? fungi comes from specimens found How far back into the geological in amber. Amber is one medium that record do fungi go … and how preserves delicate objects, such as fungal Hdo we know this? They surely do not bodies, in exquisite detail (Poinar, 2016). fossilize, right? This is due to the preservative qualities It turns out that although soft fleshy of the resin when contact is made with fungi do not fossilize very well, we do entrapped plants and animals. Not only have a fossil record for them. (Indeed, I does the resin restrict air from reaching can recommend an excellent book, Fossil the fossils, it withdraws moisture from Fungi by Taylor et al.; 2014; Academic the tissue, resulting in a process known Press.) The first fungi undoubtedly as inert dehydration. Furthermore, originated in water; estimates of their age amber not only inhibits growth of mostly come from “molecular clocks” microbes that would decay organic and not so much from fossils. Based on matter, it also has properties that kill fossil record, fungi are presumed to have microbes. Antimicrobial compounds in Figure 2. Coprinites dominicana from been present in Late Proterozoic (900- the resin destroy microorganisms and Dominican amber, 20 MYA. Photo 570 MYA) (Berbee and Taylor, 1993). “fix” the tissues, naturally embalming courtesy G. Poinar. The oldest “fungus” microfossils were anything that gets trapped there by a found in Victoria Island shale and date to process of polymerization and cross- around 850M-1.4B years old (Butterfield, bonding of the resin molecules (Poinar 2005), though the jury is still out on if and Hess, 1985). truly fungal. The first terrestrial plants George Poinar is the world’s date to around 700 million years ago authority on mushrooms found in (MYA) and the consensus seems to be amber and generously contributed that fungi probably arrived on land just a wonderful collection of images ahead of them and paved the way for (and a wealth of information) for this plants to move from marine to ever drier review. The evolutionary history of habitats. The first “lichen-like” organisms gilled mushrooms is restricted to the we see date to around 600 MYA. At relatively few fossils from Cenozoic about 550 MYA is when chytrids and and Cretaceous amber, with the oldest higher fungi split from a common specimen, Palaeoagaricites antiquus ancestor (Berbee and Taylor, 1993). The 100 MYA (Figure 1), in Myanmar first taxonomically-identifiable fungi amber showing an affinity to members are from 460 MYA, and seem similar of the family Tricholomataceae (Taylor to modern Glomeromycota, ubiquitous et al., 2015). Excellent examples of but still poorly known fungi that now gilled mushrooms in amber have thrive in all terrestrial biomes of the been published by David Hibbett and planet. At about 400 MYA is when the others, including Archaeomarasmius Basidiomycota and Ascomycota split legetti from 90 MYA and Protomycena Figure 3. Sporocarps of a wood- from a common ancestor. The first electra from 20 MYA (Hibbett et al., inhabiting species tentatively identified insects came onto the scene around 400 1997), and Aureofungus yaniguaensis as Favolaschia sp. Photo courtesy MYA; the first beetles and flies came (Hibbett et al., 2003). Gilled mushrooms G. Poinar. 10 FUNGI Volume 11:5 2019 from amber; sporophores of the puffball, Lycoperdites tertiarius, in Mexican amber (Figure 5) (Poinar, 2001) and the first known fossil bird’s nest fungi (Figures 6 and 7), where you can see the peridioles at the base of the peridia (Poinar, 2014b). The clavarioid fungus, Palaeoclavaria burmitis, in Burmese amber (Figure 8) represents the first fossil record of the non-gilled mushrooms. Not only were sclerified generative hyphae with clamp connections present, but spores borne externally on basidia could be observed (Poinar and Brown, 2003). What about ascomycetes? Yes, there have been fossils recovered that have been identified as members of the Ascomycota, even from well-known modern groups like morels and Dead Man’s Fingers. An early form of the latter, Xylaria antiqua (Figure 9), is well-preserved with organized layers of conidiophores still retaining their condia as well as perithecia filled with ellipsoid ascospores adjacent to the ostioles (Poinar, 2014a). From Dominican Republic amber we see Paleomorchella dominicana (Figure 10) (Boucot and Poinar, 2010). The specimen is a mere 2 mm in length, and thus very immature, (a) which could account for why it does not much resemble extant morels (note that there are no sponge-like pits or sterile to share characteristics found in their ridges of more familiar morels, instead descendants today (Boucot and Poinar, this ancient specimen has longitudinal 2010; Poinar and Singer, 1990). Recently ridges more reminiscent of striate discovered in Baltic amber from the or sulcate basidiomycete mushroom Samland Peninsula of Russia is an caps). And this is something worthy organism given the name Gerontomyces of pointing out: most fleshy fungi (or lepidotus (Poinar, 2016) (Figure 4). objects thought to be fleshy fungi) found The specimen was small (1.8 mm total in amber are very small, typically just length) but well-preserved and includes a few millimeters, and don’t exhibit a complete pileus (cap) just 1 mm in many easily discerned morphological diameter. The stipe (stem) is broken at characteristics. the base but still attached to the cap. Also of interest are various arthropods Due to the absence of spores and the and mycoparasites associated with (b) basal portion of the stipe, it is difficult fossil fleshy fungi. Leaving the cap of to align Gerontomyces lepidotus with Coprinites dominicana in Dominican any modern genus or even family. The amber is a mite that was trapped when Figure 4. Gerontomyces lepidotus from combination of such a small size, dry, the mushroom was preserved (Poinar Baltic amber found in Russia. a) shows brownish, scaly surface, broad, distant and Singer, 1990) (Figure 2). Adjacent side view; b) shows ventral view. Photo to subdistant lamellae (gills) and a to the Baltic amber Gerontomyces courtesy G. Poinar. straight, solid stipe are not common lepidotus was an exuvia of a nymph of a characters in gilled mushrooms, Phasmatodea (and strand of mammalian such as Coprinites dominicana although some of these features do hair) (Figure 4). It was assumed that the from 20 MYA (Figure 2), along with occur in a few genera in the family insect was feeding on the mushroom sporocarps of a wood-inhabiting species Tricholomataceae (Poinar, 2016). (Poinar, 2016). A small polypore in tentatively identified as Favolaschia There are gasteromycetes known Dominican amber that was tentatively sp. (Mycenaceae) (Figure 3), appear identified as a Ganoderma sp. is partly 2019 FUNGI Volume 11:5 11 Figure 5. Lycoperdites tertiarius, a puffball from Mexican amber. Figure 6. Fossil bird’s nest fungus, Cyathus dominicanus. Photo Photo courtesy G. Poinar. courtesy G. Poinar. eaten by an unknown agent, but still make out (Figure 1) the presence of includes many well-known mushroom- shows the outer rounded margin mycelial strands of a parasitic fungus, producing groups like Amanita, Russula, and faint pores on the undersurface Mycetophagites atrebora, that ramify chanterelles, and boletes. Additional (Figure 11) (Boucot and Poinar, 2010). through the cap. Furthermore, inside the mycorrhizal associations have arisen Two insects were associated with hyphae of the latter are hyphal strands as well, including a special kind of the fruiting bodies of Palaeoclavaria of a hyperparasite, Entropezites patricii mycorrhizae between orchids and burmitis in Burmese amber (Figure 8). (Poinar and Buckley, 2007). fungi. More on orchid fungi in the fossil One was a fungus gnat in the family Mycorrhizal relationships are believed record, below. Mycetophilidae that appears to have to have arisen more than 400 MYA Recently, the first fossil been in the process of depositing eggs as plants began to colonize terrestrial ectomycorrhiza associated with on a sporocarp. The other was a larva habitats – indeed, these fungi are flowering plants (angiosperms) was of a phlebotomine fly that was probably thought to have facilitated plants’ discovered (Beimforde et al., 2011) developing in one of the fruiting bodies move to land – and are seen as a key (Figure 12, courtesy of P. Nascimbene). (Poinar et al., 2006). The Burmese innovation in the evolution of vascular The fossils were found in a piece of amber Palaeoagaracites antiquus plants. There are two primary types of Lower Eocene (52 MYA) Indian amber, (Figure 1) mentioned above is so well- mycorrhizae: the more ancestral and from a time only 13 million years preserved that it led to the discovery predominant is called endomycorrhiza after the demise of the dinosaurs. The of mycoparasites in amber. This is the (“arbuscular mycorrhizae”), found in ECM inclusions show various stages oldest fossil mushroom, and only the over 80% of all plant species studied. of development and reveal a variety of second described from the Cretaceous The less common form is called morphological details. “Mycorrhizae are (along with Archaeomarasmius ectomycorrhiza (ECM), occurring extremely rare in the fossil record – in leggetti) (Hibbett et al., 1997). You can in roughly 10% of plant species, and fact, only one other fossil ECM has ever 12 FUNGI Volume 11:5 2019 Figure 7. Fossil bird’s nest fungus, Nidula Figure 8. The clavarioid fungus, baltica. Photo courtesy G. Poinar. Palaeoclavaria burmitis, in Burmese amber. Photo courtesy G. Poinar. been found,” Dr. Alexander Schmidt from Göttingen University (Germany), examination of the posterior end of the the senior author of the study, told seed of M.
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