An ambrosia fungus is described from filamentous sporodochia adjacent to a wood-boring ambrosia beetle (Coleoptera: Curculionidae: Platypodinae) in mid-Cretaceous Burmese amber. Yeast-like propagules and hyphal fragments of Paleoambrosia entomophila gen. nov. et sp. nov. occur in glandular sac mycangia located inside the femur of the beetle. This is the first record of a fossil ambrosia fungus, showing that symbiotic associations between wood-boring insects and ectosymbiotic fungi date back some 100 million years ago. The present finding moves the origin of fungus-growing by insects from the Oligocene to the mid-Cretaceous and suggests a Gondwanan origin. Published by Elsevier Ltd on behalf of British Mycological Society

Poinar, George O., Jr.

Vega, Fernando E.

Undetermined

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lable at ScienceDirectFungal Biology 122 (2018) 1159e1162Contents lists avaiFungal Biologyjournal homepage: www.elsevier .com/locate/ funbioA mid-Cretaceous ambrosia fungus, Paleoambrosia entomophila gen.nov. et sp. nov. (Ascomycota: Ophiostomatales) in Burmese (Myanmar)amber, and evidence for a femoral mycangiumGeorge O. Poinar Jr. a, Fernando E. Vega b, *a Department of Integrative Biology, Oregon State University, Corvallis, OR, 97331, USAb Sustainable Perennial Crops Laboratory, United States Department of Agriculture, Agricultural Research Service, Beltsville, MD, 20705, USAa r t i c l e i n f oArticle history:Received 18 July 2018Received in revised form11 August 2018Accepted 15 August 2018Available online 22 August 2018Corresponding Editor: Nicholas MoneyKeywords:Fossil fungusMycangiaNew genusNew speciesPlatypodinaeSymbiosis* Corresponding author. Fax: þ1 301 504 6491.E-mail address: Fernando.Vega@ars.usda.gov (F.E.https://doi.org/10.1016/j.funbio.2018.08.0021878-6146/Published by Elsevier Ltd on behalf of Brita b s t r a c tAn ambrosia fungus is described from filamentous sporodochia adjacent to a woodeboring ambrosiabeetle (Coleoptera: Curculionidae: Platypodinae) in mid-Cretaceous Burmese amber. Yeast-like propagulesand hyphal fragments of Paleoambrosia entomophila gen. nov. et sp. nov. occur in glandular sac mycangialocated inside the femur of the beetle. This is the first record of a fossil ambrosia fungus, showing thatsymbiotic associations between woodeboring insects and ectosymbiotic fungi date back some 100million years ago. The present finding moves the origin of fungus-growing by insects from the Oligoceneto the mid-Cretaceous and suggests a Gondwanan origin.Published by Elsevier Ltd on behalf of British Mycological Society.1. IntroductionAmbrosia beetles (Coleoptera: Curculionidae: Platypodinae) arewell known for co-habitingwith symbiotic fungi in their galleries indead and dying trees. These ambrosia fungi produce clusters ofconidia and conidiophores (sporodochia) that nourish the beetlelarvae and adults. Spores and hyphal fragments of these ectosym-biotic fungi are transported from tree to tree on the insect surfaceor in special pits, cavities, pouches (mycangia) of the adult beetles(Batra, 1967; Beaver, 1989; Harrington et al. 2010).The present study describes a newgenus of fossil ambrosia fungibased on conidiophores and conidia produced in superficial spor-odochia adjacent to an ambrosia beetle in mid-Cretaceous Burmese(Myanmar) amber. Also characterized are glandular sac mycangiacontaining hyphal fragments and yeast-like propagules in the fe-mur of the beetle. Based on the damaged elytra of the ambrosiabeetle and associated wood fragments near the beetle (Fig. 1), weVega).ish Mycological Society.propose that a predator removed the beetle from its gallery nearthe surface of the host tree, along with some wood fibers. Associ-ated with the ambrosia beetle was a symbiotic fungus and some ofits sporodochia remained appressed to the insect. Thus, the fossilprovides us with an ambrosia beetle, an associated ambrosia funguswith mycelium, conidiophores and conidia, mycangia with fungalstages, and wood fibers of the host tree.This is the first fossil record of an ambrosia beetle associatedwith its symbiotic fungus (Taylor et al. 2015) as well as the firstreport of a mycangium in the femur of any ambrosia beetle.2. Materials and methodsThe specimen originated from the Noije Bum 2001 Summit Sitemine excavated in the Hukawng Valley in 2001 and locatedsouthwest of Maingkhwan in Kachin State (26º200N, 96º360E) inMyanmar. Based on paleontological evidence this site was dated tothe late Albian of the Early Cretaceous (Cruickshank and Ko, 2003),placing the age at 97e110 million years ago (Ma). A UePb zirconstudy determined the age to be 98.8 ± 0.6 Ma or at the Albian/Cenomanian boundary (Shi et al. 2012). Nuclear magneticFig. 1. Entire beetle specimen in Burmese amber. Note associated wood fragments inbottom left portion of figure. Ambrosia fungus can be seen adjacent to the anterior endof the abdomen. Arrow points at femur containing mycangium. Scale ¼ 0.9 mm.Fig. 3. Conidiophores with apically borne conidia of Paleoambrosia entomophila gen.nov. et sp. nov. in Burmese amber. Bar ¼ 12 mm.G.O. Poinar Jr., F.E. Vega / Fungal Biology 122 (2018) 1159e11621160resonance (NMR) spectra and the presence of araucaroid wood fi-bers in amber samples from the Noije Bum 2001 Summit Siteindicate an araucarian tree source for the amber (Poinar et al. 2007).Observations and photographs were made with a Nikon SMZ-10 R stereoscopic microscope (Nikon Instruments, Tokyo, Japan)and Nikon Optiphot compound microscope (Nikon Instruments,Tokyo, Japan) with magnifications up to 800 X.3. ResultsThe Burmese amber fossil is represented by mycelium,conidiophores and conidia in sporodochia adjacent to the beetle(Figs. 1e5), and yeast-like propagules and hyphal fragments in thefemoral mycangium of the beetle (Figs. 6 and 7).TaxonomyPhylum Ascomycota (Berk.) Cavalier-Smith (1998)Class SordariomycetesOrder Ophiostomatales Benny & Kimbrough (1980)Family Ophiostomataceae Nannfeldt (1932)Paleoambrosia Poinar and Vega gen. nov.Diagnosis: as for type species (monotypic)Fig. 2. Anterior end of adult platypodine beetle in Burmese amber with sporodochia ofPaleoambrosia entomophila gen. nov. et sp. nov. Bar ¼ 380 mm.Fig. 4. Terminal cluster of four remaining conidia at the tip of a conidiophore ofPaleoambrosia entomophila gen. nov. et sp. nov. in Burmese amber. Bar ¼ 9 mm. Insertshows conidia in a mucilage head. Bar ¼ 11 mm.Fig. 5. Spore clusters of Paleoambrosia entomophila gen. nov. et sp. nov. in Burmeseamber. (A) The mucilage deposit is obvious in this spore head. Bar ¼ 5 mm. (B) Aconidium in the process of leaving the spore head. Bar ¼ 5 mm.Fig. 6. Detail of a portion of the femoral mycangium showing hyphal fragments andyeast-like propagules (arrow) of Paleoambrosia entomophila gen. nov. et sp. nov. inBurmese amber. Bar ¼ 7 mm.Fig. 7. Femoral mycangium of Paleoambrosia entomophila gen. nov. et sp. nov. in Bur-mese amber. Note two large cavities separated by a central column of glandular tissue.Arrows show openings to the exterior. Bar ¼ 18 mm.G.O. Poinar Jr., F.E. Vega / Fungal Biology 122 (2018) 1159e1162 1161Type species: Paleoambrosia entomophila Poinar and Vega sp.nov. (Figs. 1e7).Etymology: Generic name from the Greek “palaios” ¼ ancientand the Greek “ambrosia” ¼ immortal. Specific epithet from theGreek “entomo” ¼ insect and the Greek “philia” ¼ love.Description: Mycelium septate, hyaline; conidiophores un-branched, variable in length, one-celled, fuscous, 2.1e2.4 mm inwidth,bearing terminal spore clusters; conidia non-septate, straight, smooth,fuscous, globose to obovoid, length 2.7e3.5 mm, width 2.1e2.7 mm,borne in apical yellowish slime droplets. Yeast-like propagules,length 2.5e4.2 mm, and hyphal fragments present in glandular sacmycangia extending 118 mm in length and located in the femur.Diagnosis: General features of P. entomophila gen. nov. et sp. nov.,such as the shape and character of the conidiophores, conidia andspore heads, align the fossil with members of the family Ophios-tomataceae. Within this family are several genera of ambrosia fungi,with Raffaelea spp. having many features (conidia shape, size,mucilage heads) of the fossil fungus. However, the small size of theconidia of the fossil differentiate it from extant members of thegenus (Batra, 1967; Kubono and Ito, 2002; Harrington et al. 2010;Simmons et al. 2016). The fuscous hue of the conidiophores andconidia and yellowish mucilage surrounding the conidial heads(Figs. 2e5), as well as the age of the fossil and its associationwith anextinct genus of platypodine beetles, distinguishes it from all extantmembers of the Ophiostomataceae.Holotype: Holotype No. BeF-7 deposited in the Poinar AmberCollection maintained at Oregon State University, Corvallis, OR,USA.Type locality: Myanmar (Burma), state of Kachin, Noije bum2001 Summit Site amber mine in the Hukawng Valley, SW ofMaingkhwan (26º200N, 96º360E).Associated beetle: Coleoptera: Curculionidae: Platypodinae.4. DiscussionFungus-growing has been reported in three insect orders:Coleoptera (Scolytinae and Platypodinae), Hymenoptera (Attini, orleaf-cutter ants), and Blattodea (Macrotermitinae termites).G.O. Poinar Jr., F.E. Vega / Fungal Biology 122 (2018) 1159e11621162Platypodinae originated in themid-Cretaceous (119e88Ma) and arethe oldest group of fungus-growing insects (Jordal, 2015). The firstplatypodine fungus-growing tribe, the Tesserocerini, arose88.5e103.4 Ma (Jordal, 2015). Ophiostomatales originated ca.101 Ma, with fungus-growing in the Tesserocerini originating ca.86 Ma (Vanderpool et al. 2017). Fungus-growing in Attini occurred61e57 Ma (Branstetter et al. 2017), followed by termites(39.5e25.8 Ma; Roberts et al. 2016).Until now, the oldest evidence of fungus-growing behavior by aninsect was based on ca. 25 Ma fossilized termite nests in Tanzania(Roberts et al. 2016). Referring to ambrosia beetles, Roberts et al.(2016) stated: “Unfortunately, no fossil evidence, either in the formof fungal gardens or unequivocal ambrosia beetle borings, exists tovalidate molecular age estimates for ambrosia beetles or to providedirect geographic evidence onwhere this symbiosis originated.” Thepresent finding moves the origin of fungus-growing by insects fromthe Oligocene (Roberts et al. 2016) to the mid-Cretaceous based onthe age of Burmese amber specimens (110e97 Ma; see above) andsuggests a Gondwanan origin (Poinar, 2018).Glandular sac mycangia (pocket like expansions in various bodyparts) are often found in extant ambrosia beetles that bear symbi-otic fungi (Harrington, 2005). Suchmycangia play an important rolenot only in fungal transmission but also in fungal survival since evenif the conidia are coveredwithmucilage, they can still be vulnerableto desiccation. The mucilage holds the spore masses together,protects the conidia from desiccation, aids adhesion of conidia tothe exoskeleton of the beetle and keeps the spores from beingdigested in the beetle's gut (Beaver, 1989). These mycangia canoccur on various body parts, including the head, thorax and legs.They can be tube-like or shaped like pits and cavities. They oftencontain a lining of glandular cells that provide nourishment for theenclosed fungal stages. Femoral mycangia with P. entomophila gen.nov. et sp. nov. are lined with glandular cells (Fig. 7) that probablyprovided nourishment to the developing yeast-like propagules andhyphal fragments (Fig. 6). It is assumed that the contents of themycangia are stages of P. entomophila gen. nov. et sp. nov., however,it is known that more than one ambrosia species can be transportedin the mycangia of ambrosia beetles (Hulcr and Stelinski, 2017). Allmycangia found in the legs of extant beetles are restricted to thecoxae (Beaver,1989). Our findings are not only the first evidence of amycangium in an amber-preserved insect, but also the first evi-dence for a mycangium in the femur of an insect.5. ConclusionsThe Myanmar amber P. entomophila gen. nov. et sp. nov. repre-sents the only known fossil ambrosia fungus, showing that theseectosymbiotic fungi, together with their Platypodinae associates,were well established some 100 Ma. The present fossil broadensour knowledge of the diversity of fossil fungi and establishes a datefor the evolution for the Ophiostomataceae.ReferencesBatra, L.R., 1967. Ambrosia fungi: a taxonomic revision, and nutritional studies ofsome species. Mycologia 59, 976e1017.Beaver, R., 1989. Insectefungus relationships in the bark and ambrosia beetles. In:Wilding, N., Collins, N.M., Hammond, P.M., Webber, J.F. (Eds.), Insect-fungusInteractions. Academic Press, London, pp. 121e143.Benny, G.L., Kimbrough, J.W., 1980. A synopsis of the orders and families of Plec-tomycetes with keys to genera. Mycotaxon 12, 1e91.Branstetter, M.G., Jesovnik, A., Sosa-Calvo, J., Lloyd, M.W., Faircloth, B.C., Brady, S.G.,Schultz, T.R., 2017. Dry habitats were crucibles of domestication in the evolutionof agriculture in ants. Proc. R. Soc. B 284, 20170095.Cavalier-Smith, T., 1998. A revised six-kingdom system of life. Biol. Rev. 73,203e266.Cruickshank, D., Ko, K., 2003. Geology of an amber locality in the Hukawng Valley,Northern Myanmar. J. Asian Earth Sci. 21, 441e455.Harrington, T.C., 2005. Ecology and evolution of mycophagous bark beetles andtheir fungal partners. In: Vega, F.E., Blackwell, M. (Eds.), Insect-fungal Associ-ations: Ecology and Evolution. Oxford University Press, Oxford, pp. 257e291.Harrington, T.C., Aghayeva, D.N., Fraedrich, S.W., 2010. New combinations in Raf-faelea, Ambrosiella, and Hyalorhinocladiella, and four new species from theredbay ambrosia beetle, Xyleborus glabratus. Mycotaxon 111, 337e361.Hulcr, J., Stelinski, L.L., 2017. The ambrosia symbiosis: from evolutionary ecology topractical management. Annu. Rev. Entomol. 62, 285e303.Jordal, B.H., 2015. Molecular phylogeny and biogeography of the weevil subfamilyPlatypodinae reveals evolutionarily conserved range patterns. Mol. Phylogenet.Evol. 92, 294e307.Kubono, T., Ito, S., 2002. Raffaelea quercivora sp. nov. associated with mass mortalityof Japanese oak, and the ambrosia beetle (Platypus quercivorus). Mycoscience43, 255e260.Nannfeldt, J.A., 1932. Studien über die Morphologie und Systematik der nicht-lichenisierten inoperculaten Discomyceten. Nova Acta Regiae Societatis Scien-tiarum Upsaliensis 8, 1e368.Poinar Jr., G., 2018. Burmese amber: Evidence of Gondwanan Origin and CretaceousDispersion. Historical Biology. https://doi.org/10.1080/08912963.2018.1446531.in Press.Poinar Jr., G., Lambert, J.B., Wu, Y., 2007. Araucarian source of fossiliferous Burmeseamber: spectroscopic and anatomical evidence. J. Bot. Res. Inst. Tex. 1, 449e455.Roberts, E.M., Todd, C.N., Aanen, D.K., Nobre, T., Hilbert-Wolf, H.L., O'Connor, P.M.,Tapanila, L., Mtelela, C., Stevens, N.J., 2016. Oligocene termite nests with in situfungus gardens from the Rukwa Rift Basin, Tanzania, support a Paleogene Af-rican origin for insect agriculture. PLoS One 11 (6), e0156847.Shi, G., Grimaldi, D.A., Harlow, G.E., Wang, J., Wang, J., Yang, M., Lei, W., Li, Q., Li, X.,2012. Age constraint on Burmese amber based on U-Pb dating of zircons. Cretac.Res. 37, 155e163.Simmons, D.R., de Beer, W., Huang, Y.-T., Bateman, C., Campbell, A.S., Dreaden, T.J.,Li, Y., Ploetz, R.C., Black, A., Li, H.-F., Chen, C.-Y., Wingfield, M.J., Hulcr, J., 2016.New Raffaelea species (Ophiostomatales) from the USA and Taiwan associatedwith ambrosia beetles and plant hosts. IMA Fungus 7, 265e273.Taylor, T.N., Krings, M., Taylor, E.L., 2015. Fossil Fungi. Academic Press, Amsterdam,p. 382.Vanderpool, D., Bracewell, R.R., McCutcheon, J.P., 2017. Know your farmer: ancientorigins and multiple independent domestications of ambrosia beetle fungalcultivars. Mol. Ecol. 27, 277e294.

A mid-Cretaceous ambrosia fungus, Paleoambrosia entomophila gen. nov. et sp. nov. (Ascomycota: Ophiostomatales) in Burmese (Myanmar) amber, and evidence for a femoral mycangium

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A mid-Cretaceous ambrosia fungus, Paleoambrosia entomophila gen. nov. et sp. nov. (Ascomycota: Ophiostomatales) in Burmese (Myanmar) amber, and evidence for a femoral mycangium

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