Review
Speciation in fungi
Introduction
Speciation, the splitting of one species into two, is one of the most fundamental problems of biology, being the process by which biodiversity is generated. Understanding how the 1.5 millions of fungal species (Hawksworth, 1991) have arisen is of fundamental interest and has tremendous applied consequences in the cases of agricultural pathogens, emerging human diseases, or fungal species used in industry and biotechnology. Although much progress on the origin of species has been made since the book of Darwin (1859), the subject remains heavily debated.
Fungi are excellent models for the study of eukaryotic speciation in general (Burnett, 2003, Kohn, 2005), although they are still rarely included in general reviews on this subject (e.g. Coyne and Orr, 2004). First, many fungi can be cultured and crossed under laboratory conditions, and mycologists have long reported numerous mating experiments among fungal species (reviewed in Le Gac and Giraud, in press). Second, fungi display a huge variety of life cycles and geographical distributions, allowing the study of which parameters most significantly influence the speciation processes. Third, numerous species complexes are known in fungi, encompassing multiple recently diverged sibling species (e.g. Dettman et al., 2003a, Fournier et al., 2005, Johnson et al., 2005, Le Gac and Girand, in press, Le Gac et al., 2007a, Pringle et al., 2005), which allows investigations on the early stages of speciation.
Excellent reviews on the modes of speciation in fungi have already been published (Burnett, 2003, Kohn, 2005, Natvig and May, 1996), and we therefore focus mostly on recent developments. We first address the question of species definitions and species criteria and then review the patterns of speciation in fungi, situating them in the general theory as applied to eukaryotes. We focus particularly on the aspects that have not been extensively reviewed previously and/or that have seen recent and significant developments, such as sympatric speciation, cospeciation, hosts shifts, reproductive character displacement, and the time course of speciation. For other aspects, readers should refer to the previous reviews to have more exhaustive discussions and references (Burnett, 2003, Kohn, 2005, Natvig and May, 1996, Olson and Stenlid, 2002, Taylor et al., 2000, Schardl and Craven, 2003).
Section snippets
Species definition vs species criteria
To study speciation, it seems necessary to first define species. The continual proposal of new species concepts may lead one to think that there is no general agreement about what species are. To the contrary, it has been argued that all modern biologists agree that species correspond to segments of evolutionary lineages that evolve independently from one another (de Queiroz, 1998). The apparently endless dispute about species concepts stems from the confusion between a species definition
Allopatric speciation
How new species arise in nature is still a highly active field of research. It has long been believed that species originate mostly through allopatric divergence (Mayr, 1963), because extrinsic geographic barriers seemed obvious impediments to gene flow. Fungi could appear as exceptions because eukaryotic micro-organisms have long been considered to have global geographic ranges (ubiquitous dispersal hypothesis; Finlay, 2002), at least for those not dependent on a host having a restricted
Theoretical issues of sympatric speciation
In contrast to the wide acceptance of allopatric speciation, the possibility of sympatric speciation in sexual populations had long been dismissed. This is because recombination between different subsets of a population that are adapting to different resources or habitats counteracts natural selection for locally adapted gene combinations (e.g. Felsensein, 1981, Rice, 1984). Recombination indeed prevents both the building of linkage disequilibrium between adaptive alleles at different loci and
Possible cases of sympatric speciation
Compelling evidence for the sympatric divergence is extremely difficult to provide, because excluding a past period of allopatry is almost always impossible (Coyne and Orr, 2004, p. 142). Even the most famous candidate cases are still debated, such as the phytophagous insect Rhagoletis pommonella (Coyne and Orr, 2004, pp. 159–162) or the cichlid fishes in African lakes (Coyne and Orr, 2004, pp. 145–154). Evidence consistent with sympatric divergence of fungal populations driven by parasitic
Nature of reproductive isolation
As seen above, a sine qua non of speciation in sexually reproducing organisms is the decrease of gene flow between incipient species due to the development of reproductive barriers. Two types of reproductive barriers are usually distinguished, prezygotic and postzygotic, depending on their time of occurrence, before or after fertilization. In fungi having a long dikaryotic stage, nuclear fusion occurs long after individual or gamete fusion, which may render the term postzygotic ambiguous. We
Evolution of reproductive isolation
How does reproductive isolation evolve with time? This question of primary importance for the understanding of the speciation process has been investigated both theoretically and experimentally during the last decades. In the few biological models studied so far (mainly animals), some trends start to emerge (Coyne and Orr, 2004): (1) pre- and postmating isolation evolve gradually; (2) premating isolation evolves faster or at the same rate as postmating isolation; (3) postmating hybrid sterility
Speciation by hybridization
Many fungal species do not exhibit complete intersterility (Le Gac and Giraud, in press), which gives the opportunity for hybridization. Hybrid speciation is classified according to the ploidy level of the resulting individuals: when hybrids have a chromosomal number that sums that of the parental species, the process is called allopolyploid speciation, whereas hybrids with ploidy identical to that of the parents are referred to as allodiploids or homoploids.
Allopolyploids have a higher ploidy
Chromosomal speciation
Another mechanism allowing instant speciation is chromosomal speciation. The first model of chromosomal speciation (speciation due to chromosomal rearrangements) considered that if two isolated populations had fixed karyotypic differences, and that recombination between rearranged chromosomes were generating unbalanced gametes that lowered fitness, between-population gene flow could be prevented upon secondary contact (White, 1978). This model was then dismissed on the rationale that
Role of epigenetic mechanisms in speciation
Major factors responsible for postmating reproductive isolation are inherited directly as part of the parental DNA, such as rapidly evolving genes that may interact incompatibly in hybrids (the Dobzhansky–Müller model) or chromosomal rearrangements that produce segmental deletions in meiotic products. However, the recent appreciation that genetic systems function largely under epigenetic control mechanisms should let us consider that these may also be involved in reproductive isolation.
Cospeciation and host shifts
In host–parasite and host–symbiont associations, speciation in one of the interacting organisms, particularly the host, can lead to speciation in the other. As a consequence of such cospeciations, a strong congruence (topological similarity) is usually expected between the host and parasite/symbiont phylogenies. High congruence has in fact been observed in some host–parasite associations involving animals, such as gophers and lice (Hafner et al., 1994), but such patterns are not the rule. Host
Asexual fungi
In asexual fungi, the theoretical issues of species formation are completely different from those in sexual organisms. There is no recombination to break down combinations of multiple alleles adapted to a given habitat, and the selective pressure on one gene has an effect on the whole genome. Any new allele allowing adaptation on a new niche can thus give rise to a new “species”. The difficulty in asexual organisms is rather to understand if, and why, discrete entities exist that we can
Genetics of speciation
Knowing which genes are involved in reproductive isolation may help get a better understanding of speciation processes. The genetics of speciation has just begun to shed some light on the evolution of reproductive isolation, but the focus so far has been mostly on insects (Wu and Ting, 2004). Genes reported to cause premating isolation are often involved in sexual pheromones (Dallerac et al., 2000, Thomas et al., 2003), in host choice for parasites mating on their host (Dambroski et al., 2005),
Conclusion
In conclusion, important advances have been made recently on the speciation in fungi, and they have proved tractable biological models for the general study of speciation. Fungi also exhibit some specific and interesting modes of speciation, and many open questions remain which will be fascinating to explore. Recently developed analytical methods for studying past gene flow and differentiation should be useful to determine in which cases fungal speciation by specialization onto novel hosts has
Acknowledgment
We thank Pierre Gladieux for comments on a previous version of the manuscript and Jim Kronstad for initiating this review. We acknowledge the grant ANR-06-BLAN-0201.
References (120)
- et al.
RIP: the evolutionary cost of genome defense
Trends Ecol. Evol.
(2004) Speciation in parasites: host switching does not automatically lead to allopatry
Trends Parasitol.
(2006)The fungal dimension of biodiversity: magnitude, significance, and conservation
Mycol. Res.
(1991)On the failure of modern species concepts
Trends Ecol. Evol.
(2006)- et al.
Molecular phylogeny and evolution of the maple powdery mildew (Sawadaea, Erysiphaceae) inferred from nuclear rDNA sequences
Mycol. Res.
(2005) - et al.
Speciation in parasites: a population genetics approach
Trends Parasitol.
(2005) - et al.
Allopatric divergence, secondary contact and genetic isolation in wild yeast populations
Curr. Biol.
(2007) - et al.
Experimental evolution of mating discrimination in budding yeast
Curr. Biol.
(2006) - et al.
Melampsora xcolumbiana, a natural hybrid of M. medusae and M. occidentalis
Mycol. Res.
(2000) - et al.
Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade
Fung. Genet. Biol.
(2004)