The Origin of Species in Fungi
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The Origin of Species in Fungi Tatiana Giraud*, Pierre Gladieux fungal species, just like most plants and that many cryptic species exist in and Michael Hood animals, have been recognized using groups of fungi where morphological morphological characters. Since the last characteristics provide little or no *Corresponding author: century, experiments with mating crosses ability to distinguish them. For instance, Departement Genetique have also been used to assess which genealogies based upon DNA sequences et Ecologie Evolutives groups are reproductively compatible have discovered eight cryptic species Laboratoire Ecologie, Systématique with each other. These experiments within a single morphological species et Evolution revealed that crosses between some in the genus Neurospora (Dettman et UMR 8079 CNRS-UPS-AgroParisTech fungal strains were impossible even al., 2003a). In contrast to the situation Bâtiment 360, Université de Paris-Sud though they were thought to belong in Ascomycetes, DNA analyses have 91405 Orsay cedex France [email protected] The problem of speciation The origin of new species is one of the most central and persistent challenges in biology, being the process by which the great diversity of life is generated. Understanding how 1.5 million fungal species have arisen over the past 500,000,000 years is of fundamental importance, yet there are also important consequences regarding agricultural pathogens, emerging human diseases, or fungi used for agriculture, industry, and biotechnology. Although tremendous progress on the origin of species has been made since the book of Darwin’s book (1859), the subject remains heavily debated and with many recent realizations about the genetics that underlie speciation processes. To study speciation (i.e. the origin Figure 1. Armillaria species. of new species), it seems necessary to first define what a species is. All to the same species, indicating the not revealed many cryptic species in biologists more or less agree that species existence of several hidden or “cryptic” mushroom-forming basidiomycete represent different lineages that evolve species within a group known by a fungi, maybe because mating tests and independently, without freely exchanging single taxonomic name. This was the morphological characteristics of the genes (De Queiroz, 2007). This means case, for instance, in the mushrooms mushroom cap were already sufficient to that matings occurs within species, and that were once thought to be the species correctly delimitate most species (Le Gac mating between species is absent or very Armillaria mellea, but where the strains and Giraud, 2008). exceptional. This is highly applicable from North America could not mate Our modern DNA techniques have to fungi because many, although not with strains from Europe (Anderson et nevertheless revealed a much richer all, species indeed mate and undergo al., 1980; Anderson and Ullrich, 1978). diversity of fungal species than was regular sexual reproduction in nature. More recently, technological advances previously recognized, particularly In fact, the structures we enjoy eating have allowed copying and sequencing among the smaller and less conspicuous are the result of sexual development DNA from regions of fungal genomes, forms (Taylor et al., 2000). Consequently, of basidiomycete fungi, and even of which yield insights directly into the the question of how such new species some ascomycete fungi (e.g. morels and amount of genetic exchange between arise in nature has become a highly truffles). groups of organisms; in modern terms, active field of research, and fungi provide A major obstacle, particularly for this measure of genetic exchange is a most tractable model for addressing fungi, has been to recognize and central to the very definition of “species.” speciation more broadly across all delimit species in nature. Classically, Such DNA technologies have revealed Continued on page 24. FUNGI Volume 3:4 Fall 2010 23 eukaryotic kingdoms (Giraud et al., 2008; graminicola. This wheat pathogen arose of premating barriers in basidiomycete Kohn, 2005). recently, most probably during wheat mushrooms are contrasted by many It has long been believed that species domestication in the Fertile Crescent, ascomycete fungi, including numerous originate mostly through their isolation by sympatric differentiation from plant pathogens, where there are often in different geographic areas (i.e. Mycosphaerella pathogens of natural no premating barriers dependent upon “allopatric divergence”) because extrinsic grasses (Stukenbrock et al., 2007). geographic provenance. For example, geographic barriers seemed obvious closely related ascomycete species are impediments to genetic exchange. In able to mate freely when experimentally fact, among the numerous recently Nature of reproductive crossed (Le Gac and Giraud, 2008), discovered complexes of cryptic species, isolation in fungi but at least for many plant pathogenic many appear consistent with such Ascomycetes hybrids are not formed in allopatric divergence, where genetically As seen above, an essential character nature because the species are adapted isolated species occupy non-overlapping of speciation in sexually reproducing to different host plants and mating occur geographic ranges. This is the case organisms is the emergence of barriers to on or inside the plants where they grow. for instance in what was known as gene flow, i.e. mechanisms that prevent As mentioned above, such adaptation Armillaria mellea (Fig. 1), as mentioned matings from spreading genes from to the host plant can itself constitutes above, where North American and one group of organisms into another. a type of premating barrier: fungi do European strains have been shown to Two types of reproductive barriers are not mate with each other because they belong to different species (Anderson et usually distinguished, premating and cannot grow together on the same host al., 1980). Similarly, the genus Lentinula, postmating, depending on their time of plant (Giraud et al., 2006). which contains the shiitake mushrooms occurrence, before or after fertilization. Postmating barriers refer to the cultivated for centuries in China and Assortative mating is the most inviability and sterility that is often Japan, was shown to encompass seven common premating barrier, which occurs observed in hybrids. In such cases, cryptic species using genealogies based when individuals or gametes are able to crosses between evolutionary lineages on comparing DNA sequences. The bias mating partners to those that are occur and lead to the production of most ancient divergence in the Lentinula similar to themselves. Assortative mating hybrids, but they exhibit little ability to corresponded to species in the Old seems to be especially important in the grow and develop or to further produce World versus the New World, and age reproductive isolation of mushrooms, functional offpsring. For instance, of this divergence could correspond where the clamp connections between crosses among Neurospora species led to the fragmentation of the Laurasian the fungal cells that reflect the onset of to the production of few and abnormal supercontinent (Hibbett, 2001). mating and basidiocarp fructification fruiting structures (perithecia) and In contrast to the wide acceptance of are almost exclusively observed when ascospores viability was low (Dettman allopatric divergence, the possibility of the tested mycelia belong to the same et al., 2003b). Relatively few studies have speciation occurring without geographic species (Le Gac and Giraud, 2008). Such reported hybrid inviability or sterility in separation (i.e. “sympatric divergence”) assortative mating has been observed for mushrooms because the experimental had long been dismissed, particularly instance between very close species of induction of basidiocarps is often very for sexual organisms. If populations the saprophyte mushrooms in the genera difficult (unfortunately for mushroom live in the same area and can meet and Serpula, Hyphoderma, Flammulina and eaters). It is therefore difficult to analyse exchange genes, it is indeed difficult Polyporus, or between related species experimentally the progeny of hybrids in to understand how they can become of the ectomycorrhizal mushrooms mushroom-forming fungi. sufficiently isolated and diverge to Laccaria, Sistotrema and Hebeloma. An interesting and different type become new species. Even relatively However, these premating barriers of reproductive isolation is when a rare matings at each generation should are often weaker when the species do new species originates as the result cause the genetics of the two populations not live in the same geographic area, of hybridization between two extant to become homogenized, which for instance on different continents. species. This phenomenon is not would impede adaptation to different Presumably geographic isolation uncommon in fungi (Olson and resources or habitats (Maynard Smith, prevents selective pressure to prevent Stenlid, 2002). A remarkable example 1966). Theoretical models have shown, crosses between incipient species (Le is that of the rust fungus Melampsora however, that sympatric divergence Gac and Giraud, 2008), whereas when × columbiana that emerged from could be possible under certain species live in sympatry there may be hybridization of M. medusa, a parasite conditions, in particular for pathogenic selection to avoid the cost of producing of the poplar tree Populus deltoides, fungi that mate on their