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Evolution of Complex Fruiting-Body Morphologies in Homobasidiomycetes

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Evolution of Complex Fruiting-Body Morphologies in Homobasidiomycetes Received 18April 2002 Accepted 26 June 2002 Publishedonline 12September 2002 Evolutionof complexfruiting-bo dymorpholog ies inhomobasidi omycetes David S.Hibbett * and Manfred Binder BiologyDepartment, Clark University, 950Main Street,Worcester, MA 01610,USA The fruiting bodiesof homobasidiomycetes include some of the most complex formsthat have evolved in thefungi, such as gilled mushrooms,bracket fungi andpuffballs (‘pileate-erect’) forms.Homobasidio- mycetesalso includerelatively simple crust-like‘ resupinate’forms, however, which accountfor ca. 13– 15% ofthedescribed species in thegroup. Resupinatehomobasidiomycetes have beeninterpreted either asa paraphyletic grade ofplesiomorphic formsor apolyphyletic assemblage ofreducedforms. The former view suggeststhat morphological evolutionin homobasidiomyceteshas beenmarked byindependentelab- oration in many clades,whereas the latter view suggeststhat parallel simplication has beena common modeof evolution.To infer patternsof morphological evolution in homobasidiomycetes,we constructed phylogenetic treesfrom adatasetof 481 speciesand performed ancestral statereconstruction (ASR) using parsimony andmaximum likelihood (ML)methods. ASR with both parsimony andML implies that the ancestorof the homobasidiomycetes was resupinate, and that therehave beenmultiple gains andlosses ofcomplex formsin thehomobasidiomycetes. We also usedML toaddresswhether there is anasymmetry in therate oftransformations betweensimple andcomplex forms.Models of morphological evolution inferredwith MLindicate that therate oftransformations from simple tocomplex formsis about three tosix times greater than therate oftransformations in thereverse direction. A null model ofmorphological evolution,in which thereis noasymmetry in transformation rates,was rejected. These results suggest that there is a‘driven’trend towards the evolution ofcomplex forms in homobasidiomycetes. Keywords: comparative methods;corticioid fungi;molecular phylogeny 1. INTRODUCTION natefruiting bodiesare oftenproduced on the underside ofwoody substrates, where they are easily overlooked. Complex multicellular formshave arisen independentlyin There is general agreement among mycologists that several cladesof eukaryotes, including fungi,plants, ani- resupinatehomobasidiomycetes are notmonophyletic mals andstramenopiles. The repeatedevolution ofcom- (Donk1964, 1971; Ju¨lich 1981; Parmasto 1986), buttheir plex formshas beentaken as evidence that natural preciserelationships are notwell resolved.Some authors selectiontends to favour morphological elaboration have suggestedthat resupinateforms representa polyphy- (Bonner1988). Alternatively, it has beensuggested that letic assemblage ofspecies that have beenderived by theoverall increasein thecomplexity ofbiological forms reductionfrom pileate-erect forms( Ju¨lich 1981; Corner has occurredsimply becausethere is alower limit ofallow- 1991), butothers have suggestedthat resupinateforms able complexity, representedby unicellular forms,but no constitutea paraphyletic grade, from which pileate-erect upper limit oncomplexity. If so,an overall increasein formshave repeatedly arisen (Oberwinkler 1985; Parmasto complexity couldoccur by a‘passive’process, which can 1995). Recentphylogenetic studieshave conrmed that beconceptualized as diffusion through morphospace resupinatetaxa are intermingled with pileate-erect taxa in (McShea1994, 1996). Muchof the debate concerning anumberof cladesof homobasidiomycetes (Hibbett et al. trendsin theevolution oforganismal complexity resides 1997; Hibbett &Thorn 2001; Langer 2002), butso far in thepalaeontological literature andconcerns morpho- therehas not,to our knowledge, been an analysis with logical evolutionin animals (e.g.Gould 1988; Wagner sufciently broad sampling toresolve theoverall pattern 1996; Sidor 2001). ofevolution offruiting-body forms. Within thefungi, some of the most conspicuous and Our studyhad three main objectives:(i) toinfer broad elaborate formsthat have evolved are thefruiting bodies phylogenetic relationships among resupinateand pileate- ofhomobasidiomycetes. Familiar examples includegilled erecthomobasidiomycetes; (ii) toestimate theancestral mushrooms,polypores, coral fungi,puffballs andstink- fruiting-body morphology ofthe homobasidiomycetes; horns(hereafter, ‘ pileate-erect’forms). Nevertheless, and(iii) todetermine whether the rate oftransformations homobasidiomycetesalso producerelatively simple from resupinateto pileate-erect formsis differentfrom the ‘resupinate’forms, which lie at ontheir substrates. rate oftransformations in thereverse direction. Resupi- Resupinatefruiting bodiesrange from ‘athelioid’forms, nateforms are morphologically simple relative topileate- which consistonly ofsparsenetworks of fertile hyphae, to erectforms becausethey are notdivided into a cap and more robust,crust-like or eshyforms that have smooth, stalk or other discreteparts, andthey have simple ridged,toothed or poroid spore-bearing surfaces.Resupi- ontogeniesthat donot include the production of veils or other protective tissuesthat are commonamong pileate- erectforms. We used maximum likelihood (ML)to esti- *Authorfor correspondence ([email protected]). mate asimple modelof evolution ofhomobasidiomycete Proc.R. Soc.Lond. B (2002) 269, 1963–1969 1963 Ó 2002 TheRoyal Society DOI10.1098/ rspb.2002.2123 1964D. S.Hibbettand M. Binder Evolution of complex morphologies in fungi * Christiansenia pallida Tremellales * Boletus retipes (a) Guepinia spathularia Xerocomus chrysenteron Femsjonia sp. Boletus satanas Dacryomitra pusilla Phylloporus rhodoxanthus * Ditiola radicata Paragyrodon sphaerosporus Dacryopinax spathularia Calostoma cinnabarina Calocera cornea Dacrymycetales Scleroderma citrinum Cerinomyces grandinioides Suillus luteus Dacrymyces chrysospermus Suillus sinuspaulianus Bolete Dacrymyces sp. Suillus cavipes Dacrymyces stillatus Chroogomphus vinicolor clade Basidiodendron caesiocinereum # Gomphidius glutinosus Basidiodendron sp. Rhizopogon subcaerulescens Bourdotia sp. # Coniophora arida # Heterochaete sp. Auriculariales Coniophora puteana Serpula himantioides # * Auricularia auricula judae Exidia thuretiana # Tapinella atrotomentosa Gastrosporium simplex Tapinella panuoides Anthurus archeri Pseudocolus fusiformis Jaapia argillacea Sphaerobolus stellatus Dendrocorticium polygonioides # Jaapia Geastrum saccatum Dendrocorticium roseocarenum Geastrum sessile Gomphoid Punctularia strigoso zonata # Dendrocorticium Ramaria stricta Vuilleminia comedens Clavariadelphus pistillaris Galzinia incrustans clade Ramaricium alboflavescens –Phalloid clade Tomentella ferruginea # * Gautieria otthii Tomentella stuposa Gomphus floccosus Tomentella coerulea * Ramaria formosa Thelephora sp. Ramaria obtussisima Thelephora palmata Uthatobasidium fusisporum # Thelephora vialis Thelephoroid Uthatobasidium sp. Hydnellum sp. Thanatephorus practicola # Sarcodon imbricatus clade Tulasnella sp. Bankera fuligineoalba Tulasnella pruinosa Phellodon tomentosus Tulasnella sp. Pseudotomentella mucidula Botryobasidium candicans Pseudotomentella nigra # Botryobasidium vagum # Pseudotomentella ochracea Botryobasidium subcoronatum Gloeophyllum sepiarium Botryobasidium isabellinum # Cantharelloid Heliocybe sulcata Gloeophyllum clade Botryobasidium sp. clade Neolentinus dactyloides Botryobasidium sp. # Hyphodontia gossypina Clavulina cinerea Subulicystidium longisporum # Paullicorticium Sistotrema eximum # Tubulicium vermiculare Sistotrema sernanderi Paullicorticium niveocremeum # clade Multiclavula mucida Sistotremastrum sp. Sistotrema brinkmannii # Bjerkandera adusta Sistotremastrum niveocremeum Phanerochaete chrysosporium # Hydnum repandum Phanerochaete sordida Hydnum rufescens Sistotrema musicola # Cantharellus cibarius Pulcherricium caeruleum Cantharellus tubaeformis Phlebiopsis gigantea # Craterellus cornucopioides Ceraceomyces serpens * Phlebia albomellea # Gerronema marchantiae Ceriporiopsis subvermispora Sphaerobasidium minutum # * Cystidiodontia isabellina # * Resinicium bicolor * Ceriporia purpurea Byssomerulius sp. Hyphodontia alutaria # Oxyporus populinus * Gloeoporus taxicola Subulicium sp. # * Ceriporia viridans Tubulicrinis sp. Ceraceomyces eludens # Hyphodontia pallidula # Ceraceomyces microsporus Schizopora flavipora Lindtneria trachyspora # * Hyphodontia cineracea Grifola frondosa * Hyphodontia alutacea # Gelatoporia pannocincta Hyphodontia palmae Candelabrochaete septocystidia * Basidioradulum radula # Climacodon septentrionalis * Tubulicrinis gracillimus Phlebia radiata # * Tubulicrinis subulatus # Mycoacia aurea Coltricia perennis Phlebiella griseofulva Phellinus gilvus Hymenochaetoid Mycoacia aff fuscoatra # * Hymenochaete corrugata clade Peniophora sp. # Hymenochaete rhabarbarina Scopuloides hydnoides Inonotus hispidus Phanerochaete chrysorhiza # Phellinus igniarius Candelabrochaete africana # Phylloporia ribis Phanerochaete sanguinea # Fibricium rude # Steccherinum fimbriatum Trichaptum abietinum Junghuhnia nitida Hyphodontia aff. breviseta Antrodiella romellii # Hyphodontia nespori Albatrellus syringae # Hyphodontia crustosa * Meripilus giganteus Hyphodontia sambuci # Hyphoderma setigerum # Hyphodontia nudiseta # Hyphoderma nudicephalum Hyphodontia aspera Hyphoderma definitum # Hyphodontia serpentiformis # Panus rudis Schizopora paradoxa Spongipellis pachyodon Hyphodontia niemelaei Hypochnicium sp. # Hyphodontia radula # Hypochnicium geogenium Polyporoid Gloeocystidiellum leucoxantha # Hypochnicium eichleri # Stereum annosum Hypochnicium polonense clade
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