Species and Speciation in Mushrooms Author(s): Ronald H. Petersen and Karen W. Hughes Source: BioScience, Vol. 49, No. 6 (June 1999), pp. 440-452 Published by: University of California Press on behalf of the American Institute of Biological Sciences Stable URL: http://www.jstor.org/stable/10.1525/bisi.1999.49.6.440 . Accessed: 13/07/2011 12:47 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at . http://www.jstor.org/action/showPublisher?publisherCode=ucal. 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Hughes It is really laughable to see what Classification of the major groups differentideas are prominent in vari- For these the of fungi is based on aspects of their ous naturalists' minds when they fungi, sexual reproductive cycle. Thus, as- speak of species; in some, resem- the ed- blance and should comycetes (including highly is everything descent of species concept ible truffles and morels as well as little weight-in some, resemblance seems to for and Cre- be grounded in a Neurospora, widely used in genetic go nothing, meiotic in a ation the reigning idea-In some, studies) produce spores descentis the key,-in some, steril- demonstration of sac called an ascus. Basidiomycetes ity an unfailingtest, with othersit is (the mushrooms and their relatives) not worth a farthing.It all comes, I phenetic cohesiveness, produce meiotic products from a believe, from trying to define the common microscopic club-shaped structure indefinable.(Letter from Darwinto evolutionary called a basidium. The zygomycetes Hooker, 24 December 1856; Dar- (black bread molds) form sexual win descent, and reproductive 1887, p. 88) spores as an elaborately ornamented isolation where possible zygosporangium. Fungi that do not is the processby which reproduce sexually are placed in an Speciationa cohesive of genetically group artificial group, the Deuteromycetes individuals di- interbreeding to whether two groups are different ("imperfect fungi"). In discussing into two or more verges genetically species or just locally adapted but species concepts and speciation pro- distinct of individuals. A groups req- interbreeding groups within a spe- cesses in this article, we emphasize uisite in this is a hiatus in process cies (Figure 1). Because speciation is the basidiomycete fungi. between the two gene exchange a process that occurs over time, there This hiatus allows emerging groups. is uncertainty concerning the exact accumulate Speciesconcepts in fungi each group to genetic point in this process when a popula- differences the natural through pro- tion becomes a species. "Species concepts" are the philo- cesses of muta- evolution, including Fungi pose special problems in sophical criteria through which and drift. When tion, selection, genetic determining species status because investigators communicate their defi- two groups have become sufficiently little is known about what consti- nition of the term "species." Con- are as different, they recognized spe- tutes an individual; the extent of versely, species concepts are not the cies. In fruit- many cases, however, variation within populations is taxonomic characters used to distin- differences are body phenotypic largely unexamined; fungi often have guish a particular species from other subtle and there is as disagreement complex, varied life cycles, each stage species. Implicit in most species con- Ronald H. Petersen(e-mail: repete@utk. of which may be subject to different cepts is the idea that two species are edu) and Karen W. Hughes (e-mail: evolutionary pressures; and repro- genetically distinct from each other [email protected]) are professors of duction (sexual and asexual) is ex- and are reproductively isolated, ei- at the of Botany University Tennessee, tremely complex and may affect evo- ther by intrinsic reproductive barri- Knoxville, TN 37996-1100. After many in that we ers or of Petersenhas lutionary patterns ways (i.e., genetic incompatibility) years morphotaxonomy, do not understand. For extrinsic factors, such as ecology investigated mating systems in mush- yet many by rooms for over a decade. is a fungi, the sexual stage of their life of the organism or geographical sepa- Hughes of geneticist with interests in the evolution cycle is unknown and, in fact, may ration. Each group organisms for and biogeography of populations. ? not exist. Many species of Penicil- poses special problems investiga- 1999 American Institute of Biological lium, from which penicillin is de- tors, and species concepts that have Sciences. rived, are amorig such fungi. been developed for one group of or- 440 BioScience Vol. 49 No. 6 University of California Press is collaborating with JSTOR to digitize, preserve, and extend access to BioScience ® www.jstor.org ganisms may not be workable for another group, although numerous Sexual attempts have been made to find A species concepts that are broadly Species applicable across kingdoms (Carson incompatibitySpecies 1985, Mayden 1997). Numerous species concepts exist, all of which 9 have their proponents and detrac- A tors (see Mayden 1997). The three Subspecies Subspecies B species concepts that are most appli- aI cable to fungi are the "morphologi- cal" species concept (i.e., differences in morphology reflect underlying RaceHRace~or A orRcB im- genetic differences and can thus Sibling Species A B ply a genetic hiatus between two Sibling Species groups), the "phylogenetic" species concept (i.e., populations may be grouped and ranked as species only Interbreedingpopulation if they share a common evolutionary lineage, usually expressed as a termi- nal node on a phylogenetic tree), and Genetic Divergence - the "biological" species concept (i.e., 0 the ability of individuals in two groups to interbreed). Figure 1. Interbreedingpopulations may diverge genetically over time until specia- tion occurs. Sexual occur to The incompatibility may quickly, leading sibling species morphological species concept. with little genetic divergence; may accompany the gradual genetic divergence; or In this concept, characters (pheno- may not develop, even between populations judged sufficiently divergent to be types)of individualorganisms are com- designated species. pared,and similarindividuals are des- ignated as a species. Inherentin this construction is an assumed genetic are appropriateand then lasting only used-is the primarycriterion defin- hiatusbetween dissimilarorganisms. a short time. The result of these prob- inga species(Mayden 1997). In prac- Decisions about similarity and dis- lems has been an intuitive classifica- tice, however,these groupsmay or similarity of characters, of course, tion, with each taxonomist grouping maynot reflectthe evolutionaryhis- are left to the taxonomist. Tradi- and ranking specimens in his or her tory of the species. tionally, characters used to identify own way. mushrooms and their relatives have Other characters have recently The phylogeneticspecies concept. been taken from the macro- and mi- been added to the repertoireof traits The phylogenetic species concept cromorphology of the basidioma (i.e., used to estimate species status of (Hennig1966), by contrast,requires the fruitingbody or mushroom).It is fungi. Fungi are often potent pro- that speciesrepresent monophyletic little wonder, then, that mushroom ducers of secondary metabolites (in- groups(i.e., the productof a single systematicshas been informedby the deed, many drugs and antibiotics are evolutionarylineage or the terminal morphological species concept (see derived from fungi). Analysis of sec- taxa on a cladogramestimating an Smith 1968, Clemenqon1977). ondary metabolites has identified evolutionarylineage). Although cla- The use of morphology to deter- relationships between morphologi- dogramsare often DNA based,they minespecies boundariesin fungi has, cally divergent groups of fungi (Gill can be developedfrom any available however, proven inadequatefor sev- and Steglich 1987, Whalley and data, includingmorphological data. eral reasons: all charactersare based Edwards 1987). In addition, electro- Most modernphylogenetic species on only one part of the life cycle, the phoretic analysis of isozymes is now conceptssupport the idea that spe- fruitbody; the mushroom fruitbody being used to evaluate population cies lie on the boundarybetween is relatively simple, so limited