Speciation in fungal and oomycete plant pathogens.

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Review in Advance first posted online on May 30, 2014. (Changes may still occur before final publication online and in print.)

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Annu. Rev. Phytopathol. 2014.52. Downloaded from www.annualreviews.org by College of William & Mary on 06/13/14. For personal use only.

Speciation in Fungal and Oomycete Plant Pathogens Silvia Restrepo,1 Javier F. Tabima,2 Maria F. Mideros,1 2 Niklaus J. Grunwald, and Daniel R. Matute3,4 ¨ 1

Departamento de Ciencias Biologicas, Universidad de Los Andes, Bogotá, Colombia ´

2

Horticultural Crops Research Laboratory, United States Department of Agriculture, Agricultural Research Service, Corvallis, Oregon 97333

3

Department of Human Genetics, University of Chicago, Chicago, Illinois 60637

4

Biology Department, University of North Carolina, Chapel Hill, North Carolina 27599p; email: [email protected]

Annu. Rev. Phytopathol. 2014. 52:14.1–14.28

Keywords

The Annual Review of Phytopathology is online at phyto.annualreviews.org

speciation, reproductive isolation, population genetics, hybrids, genomics

This article’s doi: 10.1146/annurev-phyto-102313-050056

Abstract

c 2014 by Annual Reviews. Copyright All rights reserved

The process of speciation, by definition, involves evolution of one or more reproductive isolating mechanisms that split a single species into two that can no longer interbreed. Determination of which processes are responsible for speciation is important yet challenging. Several studies have proposed that speciation in pathogens is heavily influenced by host-pathogen dynamics and that traits that mediate such interactions (e.g., host mobility, reproductive mode of the pathogen, complexity of the life cycle, and host specificity) must lead to reproductive isolation and ultimately affect speciation rates. In this review, we summarize the main evolutionary processes that lead to speciation of fungal and oomycete plant pathogens and provide an outline of how speciation can be studied rigorously, including novel genetic/genomic developments.

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INTRODUCTION


The major evolutionary forces that lead to the emergence of new plant-pathogen species remain largely unknown; however, based on our understanding of speciation in general and from case studies of particular fungi or oomycetes a clearer picture is beginning to emerge. Understanding the demographic and ecological factors that lead to the evolution of plant-pathogen species can greatly advance our knowledge of how they adapt to agricultural systems and provide new insights for plant disease management. In addition to these potential applications, fungi and oomycetes are ideal models for understanding the biological features that lead to new species in general. Fungi and oomycetes comprise a large number of species (Oomycota: ∼800 species; Fungi: ∼70,000 species) (90), of which many can cause disease in a wide variety of plant hosts. These factors make them appealing models for evolutionary biologists because pathogen biology provides an extraordinary window into how species interactions shape divergence patterns in different organisms and allows for clear hypotheses formulation. For example, given the dependence of plant pathogens on their host species, it is expected that some of the major mechanisms underlying plant-pathogen species emergence include host-range expansion and host jumps (21, 70, 181). Following human migrations, host-range expansion might have been largely the result of migration or movement of pathogens or hosts into new geographic regions (18, 22, 56). Nonetheless, many of these hypotheses remain largely untested. A unified conceptual framework to properly define the biological features that give rise to new species, allow persistence over time, and characterize the divergence processes in plant pathogens is needed. Our aim here is twofold: (a) We want to summarize the current evidence for how new plant-pathogen species emerge, and (b) we want to outline a rigorous framework for characterizing the divergence, hybridization, and speciation observed in these organisms.

SPECIATION IN PLANT PATHOGENS: THE ROLE OF REPRODUCTIVE ISOLATION Evolutionary biologists have long studied the evolutionary processes that give rise to new genotypes, lineages, and eventually species, as well as the traits that make species unique (33, 147). Species are the largest and most inclusive reproductive community of cross-fertilizing individuals that share a common gene pool (45). This definition, known as the biological species concept, was coined to delimitate species boundaries in a hypothesis-testing framework. At its core, it has a simple premise: If two individuals show biological features that reduce or eliminate the possibility of gene flow between them, then they belong to different species. Importantly, speciation is a continuous process in which lineages diverge gradually to form separate species. On the surface, this definition does not seem to apply to clonal lineages because the potential for recombination and gene flow is not thought to exist. Nonetheless, alternative approaches have been proposed to detect the signature of reproductive isolation in these organisms (61, 124). Because gene flow is a homogenizing force that reduces genetic and phenotypic differences between groups of individuals, reproductive isolation must be a key feature of the process of speciation (and/or of species maintenance), even among asexual species. The appeal of this definition is twofold. First, it links species boundaries with the processes that lead to the evolution of traits that preclude gene flow between groups of individuals. Second, it provides a conceptual framework for recognizing species boundaries that allows for rigorous hypothesis testing: If gene flow between demes is reduced or nonexistent, then there must be reproductive barriers between the groups. Studying the processes involved in speciation thus boils down to understanding the barriers to genetic exchange and the mechanisms that shape these barriers. 14.2

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These mechanisms can be classified into three main groups depending on where they occur in the reproductive cycle: premating, postmating-prezygotic, and postzygotic isolation (33, 46). Table 1 lists the reproductive isolating mechanisms (RIMs) that have been previously described in fungal and oomycete plant pathogens. Some major trends emerge from this literature review. Premating isolating barriers are by far the most often reported RIMs to date in plant pathogens (Table 1). Ecological isolation, especially by host specialization between potentially recombining species is reported as the most widespread form of reproductive isolation (177, 188) (Table 1). This observation might constitute an ascertainment bias because plant-pathogen research usually starts by investigating host range. However, ecological isolation is not the only type of reproductive isolation reported for plant pathogens (Table 1). Interspecific crosses between species of Phytophthora induce fewer sexual structures than intraspecific crosses, which indicates the existence of premating isolating mechanisms that hinder the production of hybrid progeny (170, 171). Postzygotic isolation, which reduces fitness of recombining individuals, has been less studied than ecologically based reproductive isolation in plant pathogens. It is clear that hybridization occurs in different groups of fungi and oomycetes (165). Extrinsic postzygotic isolation by reductions of hybrid fitness due to ecological factors seems to be common in plant pathogens. Hybrids between highly specialized pathogens that might not fare well in any of the parental niches consequently show low fitness in parental niches (see examples in section “Ecological Divergence” below) (70). However, some interspecific hybrids can have profound economic implications for agriculture, have a higher fitness than either parental (hybrid vigor), and show changes or expansions of host ranges (165). It remains unclear how frequently hybridization leads to range expansion or host jumps (64) as well as how frequently interspecific hybrids show decreased ecological fitness and are outperformed by the parental species. A second type of postzygotic isolating mechanism relates to the viability and fertility of the resulting hybrids and has been termed intrinsic reproductive isolation. This type of RIMs has been heavily studied in other taxa (137, 185, 192), but reports of their existence in plant pathogens are scarce. Examples of hybrid sterility have been documented for species of the genera Mycrobotryum (44, 113), Ascochyta (105), and Cochliobolus (131, 132), as well as in Gibberella zeae (17, 104), among others. The most extreme phenotype, hybrid inviability, has also been documented for species of the genera Ceratocystis (50, 88) and Phytophthora (41, 54, 129). It is crucial to understand how pervasive postzygotic mechanisms are given the substantial importance of host specialization in plant pathogens. An additional RIM in fungi and oomycetes is somatic incompatibility (SI) (117, 194). Mycelia from fungi and oomycetes can fuse vegetatively and give rise to hybrid individuals. SI is a system by which filamentous fungi can distinguish their own mycelia from those of other individuals and from individuals of different species. Even though SI occurs in several taxa, it has received little attention in the field of speciation research (118, 194). SI is of special importance for the generation of new genetic variation (reviewed in 139), especially in organisms for which sexual cycles do not exist or have yet not been observed. In somatic fusion between organisms of different species, hybrid individuals could be produced that might allow for gene flow between parental species. Similar to barriers to sexual reproduction, there can be barriers to the fusion of somatic tissues, especially when individuals belong to divergent parental species; such barriers are found between different populations and species of cereal rusts (Puccinia spp.) (117). Somatic barriers to gene flow can also act at different steps in the somatic fusion process (failure of anastomoses, genetic, and cytoplasmatic incompatibilities) (117, 194). Even though SI is unlikely to lead to speciation, it might have a role in keeping species apart. SI is doubtlessly important for stopping gene flow between individuals, populations, and ultimately species, so its role in plant pathogens needs to be studied further. www.annualreviews.org • Speciation in Fungal and Oomycete Plant Pathogens


RIMs: reproductive isolating mechanisms Hybrid vigor: higher fitness observed in some hybrids arising from interspecific crosses; also called heterosis Intrinsic reproductive isolation: RIMs that are not dependent on the environment (unlike extrinsic reproductive isolation). Hybrid inviability and sterility are examples of intrinsic RIMs SI: somatic incompatibility

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Table 1 Reproductive isolating mechanisms observed in fungi and oomycete plant pathogens. Pairs of taxonomically recognized species are shown in two columns. Species complexes are shown in a single columna


Species 1

Type of isolating mechanism

Method and conclusions

Reference

Phytophthora infestans

Phytophthora mirabilis

Premating

In vitro interspecific crosses failed to produce hybrids

(79)

Phytophthora rubi

Phytophthora fragariae

Premating

Attempts to infect each other’s host have been unsuccessful

(120)

Phytophthora capsici

Phytophthora tropicalis

Postmating, prezygotic

In vitro interspecific crosses revealed the existence of hybrid sterility

(47)

Phytophthora megakarya

Phytophthora nicotianae

Postmating, postzygotic

In vitro interspecific crosses produced fewer progeny than conspecific crosses and inviable oospores

(14)

P. capcisi

Phytophthora nicotianae

Postzygotic

In vitro interspecific crosses produced mostly inviable oospores

(14)

P. capcisi

Phytophthora palmivora

Postzygotic


(14)

Phytophthora vignae

Phytophthora sojae

Postmating postzygotic

Interspecific crosses in vitro and infection assays showed that F1 hybrids have reduced aggressiveness.

(121)

Phytophthora infestans

Phytophthora palmivora

Premating

Absence of natural hybrids in areas of secondary contact. Possible reproductive isolation

(163)

Phytophthora parasitica

Phytophthora cinnamomi

Premating


(15)

P. parasitica

Phytophthora megakarya

Premating


(55)

P. sojae

Phytophthora medicaginis

Premating

Putative species were isolated in different substrates, indicating habitat isolation

(87)

Phytophthora porri

Phytophthora brassicae

Premating


(40)

P. cinnamomi

Phytophthora cambivora

Premating


(14)

Microbotryum violaceum complex


In vitro interspecific crosses revealed the existence of hybrid sterility

(44)

M. violaceae complex

Premating and postmating, postzygotic

Interspecific crosses in vitro and infection assays indicated that F1 hybrids have lower fitness than parental species

(113)

Prezygotic


(188)

Ophiostoma piceae complex

Premating


(142)

Cylindrocladium floridanum

Premating

Interspecific crosses failed to produce hybrids

(106)

Melampsora medusae f. sp. deltoidae

Species 2

M. medusae f. sp. tremuloidae

Cylindrocladium canadence

(Continued )

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(Continued ) Type of isolating


Species 1

Method and conclusions

Reference

C. floridanum

Cylindrocladium pacificum

Premating


(106)

C. floridanum

Cylindrocladium pseudospataphylli

Premating


(106)

Ascochyta rabiei complex (Ascochyta fabae, Ascochyta lentis, Ascochyta pisi, A. rabiei, and Ascochyta viciae-villosae)

Premating and postmating

Host specificity assays revealed habitat isolation; inoculations with F1 hybrid spores suggested reduced fitness of the hybrids in the habitat of both parentals

(93)

Didymella rabiei demes from two different chickpeas


Thermal fitness differences indicated possible habitat isolation; inoculations with F1 hybrid spores suggested reduced fitness of the hybrids in the habitat of both parentals

(62)

Microbotryum lychnidis-dioicae


Interspecific crosses in vitro revealed the existence of hybrid sterility

(44)

Melampsora lini species complex

Premating

In vitro interspecific crosses in vitro detected vegetative incompatibilities

(59)

Fusarium oxysporum

Postmating


(32)

Gibberella fujikuroi (Fusarium moniliforme)

Premating


(149)

P. cinnamomi



(171)

Phytophthora drechsleri, P. cinnamomi, P. parasitica, P. palmivora

Premating

Interspecific crosses in vitro detected hybrid inviability and sterility

(170)

A. fabae/A. lentis

Postzygotic

In vitro interspecific crosses revealed hybrid sterility

(93, 105)

Gibberella zeae (Fusarium graminearum) species complex

Postzygotic

In vitro interspecific crosses revealed hybrid sterility

(17, 104)

Fusarium acuminatum, Fusarium avenaceum, Fusarium culmorum, Fusarium crookwellense, F. oxysporum

Postzygotic

In vitro interspecific crosses revealed hybrid sterility and inviability

Phytophthora alni


Lower fertility in interspecific crosses; hybrids showed reduced growth rate

(43)

Ceratocystis fimbriata, Ceratocystis cacaofunesta, Ceratocystis platani


In vitro interspecific crosses revealed hybrid inviability

(50)

Ceratocystis coerulescens

Premating


(89)

a

Species 2

Microbotryum silenes-dioicae

mechanism

A total of 34 species pairs have been studied and six RIMs have been reported between them (36 papers).

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a

Locus 1

c

Locus 3

b

Locus 2

d

Locus 4

e

Species tree

Dxy

π1

π2

Figure 1 Recognizing species in plant pathogens. Gene genealogies can be used to reconstruct the phylogenetic history of sister species. Four hypothetical loci (a–d ) were used to build the genealogies shown in each panel. The size of each circle is proportional to the number of individuals that show a particular haplotype (black dots represent missing haplotypes and are a proxy of genetic distance between observed haplotypes). The goal of building gene genealogies is to identify potential speciation events and discern whether gene flow is still ongoing. In this example, the four loci depict the evolutionary history of two hypothetical species (Sp1, red; Sp2, yellow). The merged data set (e) can be used to calculate the intraspecific polymorphism (π) and the absolute divergence (i.e., Dxy). These quantities can be compared to determine how much divergence has accumulated between the two species.

SPECIES RECOGNITION IN PLANT PATHOGENS Because reproductive isolation is often not easily assessed, fungal and oomycete species have traditionally been defined with morphological and phenotypic traits. Contemporary species description integrates these classical approaches with sequence-based phylogenetic approaches that attempt to find evidence of reproductive isolation (8, 26, 34, 84, 98, 133). The premise of such approaches is that different gene genealogies of two groups that have ceased interchanging genes should reflect concordant topologies among loci. The most common practice involves the use of gene genealogies to detect long branches, which in turn can be interpreted as discontinuities in population structure that might signal lack of gene exchange (depicted in Figure 1). Such studies have revealed that the number of species in fungi and oomycetes tends to be underestimated by a factor of two (96, 110, 183, 184). In an attempt to unify molecular taxonomy, some general guidelines have been proposed as to what levels of divergence are required to designate species 14.6

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in fungi (42, 43), although how these correlate with reproductive isolation is unknown. Accordingly, species description should rely on multiple, unlinked loci from neutrally evolving genes with strong phylogenetic signals (5, 24, 141, 162). Figure 1 shows an example of the use of gene genealogies to reconstruct the divergence history of a pair of cryptic sibling species. Phylogenetic species recognition practices and the application of other species concepts are extensively reviewed elsewhere (25, 154). Identifying species is a challenging task for asexual populations. The majority of species concepts have been developed for individuals that reproduce sexually and recombine with individuals from the same gene pool. Thus, a rigorous framework is required to study species formation in those groups of organisms that do not reproduce sexually or for which no sexual stage is known. Population genetics and evolutionary theory for asexual taxa provide some guidance and several quantitative extensions of the gene genealogies approach have been proposed. Two of the most comprehensive proposals are the K/θ method (or 4X rule) and the application of branching rates in phylogenetic trees. The K/θ method (12) uses DNA polymorphism and basic coalescent theory to identify clusters of organisms that are diverged enough to be considered separate species. The average number of differences between individuals of two species (after correcting for multiple hits) equals, on average, 8Ne μ, where Ne is the effective population size and μ is the mutation rate (7). This quantity is known as K. Intraspecific polymorphism, θ, is roughly equivalent to 2Ne μ. The K/θ metric reflects divergence scaled by the effective population size and is thought to reveal different species if greater than 4, hence the reference to the 4X rule. This approach identifies putative species only on the basis of reciprocal monophyly using rooted trees and ascribes a metric to delimitate populations from true species (11, 156). An alternative framework for considering whether a clade has diversified into discrete genetic clusters is to consider branching models in phylogenetic trees (145). This approach is more complex than the K/θ method but allows for a global test of the relative rates of divergence within a clade. Under a null model, the entire sample derives from a single asexual population, i.e., without divergence into independently evolving or ecologically distinct species. Under this null hypothesis, the pattern of branching is expected to conform to a standard coalescent model for a single population. However, if speciation has taken place, the branching pattern of a phylogenetic tree deviates from the coalescent null hypothesis and has longer branches in the deeper regions of the phylogenies. These long branches are thus a diagnostic that reveals species boundaries. A large body of theoretical work is available to specify the likelihood of a given pattern of branching under a particular model (107), ranging from a neutral coalescent in a population of constant size to populations that increased through time or experienced different forms of selection (157). To our knowledge, this approach has not been applied to plant pathogens but, along with the K/θ method, has the potential for application to the identification of species boundaries and determination of rates of speciation.

Effective population size (Ne ): the size of an idealized population that would have the same population genetic properties of the population under study

HOW TO STUDY SPECIATION IN PLANT PATHOGENS? The completion of speciation is signaled by the existence of distinct RIMs. Thus, understanding how species originate necessarily focuses on understanding what biological features prevent gene flow. Although research in plant pathology is usually not characterized as speciation research, a series of approaches has aimed at dissecting the biological basis of reproductive isolation between plant-pathogen species. We divide these studies into two categories and refer to the studies that have identified RIMs between species as the classical studies. The second category, genomic studies, involves genome-scale studies that identify genomic features that are involved in reproductive isolation or in interspecies differences. There is no reason, however, for these categories to be www.annualreviews.org • Speciation in Fungal and Oomycete Plant Pathogens


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distinct, and we are optimistic that the coming years will see an increase in studies that combine both of these approaches.

Classical Studies


Because one of the most notable traits of plant pathogens is their habitat specificity, most of the studies dealing with reproductive isolation have addressed the possibility of isolation by ecological factors, such as reciprocal fitness in each other’s niches (common garden or transplant experiments) in two species that share a most recent common ancestor. In multiple cases (31), these experiments have demonstrated the existence of extreme specialization to plant hosts. In these instances, the main source of reproductive isolation is likely to be the separation of nascent species by these ecological factors. For example, species of the genus Ascochyta (teleomorph Didymella) (93, 105) show strong ecological isolation. Inoculations with ascospores from Ascochyta fabae caused disease in fava bean but not in lentil; inoculations of ascospores from Ascochyta lentis caused disease in lentil but not in fava beans, indicating strong host specificity and ecological isolation. The crosses between the two species produced fewer ascospores per ascus than pure species crosses, indicating the existence of a postmating nonecological RIM. Moreover, inoculation with hybrid ascospores (A. fabae × A. lentis) did not induce disease in either host. This suggests a fitness depression in the hybrids and the presence of extrinsic postzygotic isolation, and demonstrates an important role of environmental factors in keeping these species apart (105). Abiotic factors can also play a role in keeping species apart. Botrytis pseudocinerea, a recently identified species, and Botrytis cinerea show adaptation to different temperatures [as measured by at least one thermal fitness component (number of sclerotia in minimal media at different temperatures), which might explain the relative abundance of B. pseudocinerea in the springtime. This temperature adaptation might also cause temporal isolation, but this has not been tested. A strong influence of temperature has been reported for ecotypes of the species complex (189). This is also the case for Phytophthora drechsleri, where northern isolates thrive in cooler temperatures and southern isolates thrive in higher temperatures (172). It is still unclear whether these ecotypes are different species and whether there are any other RIMs between them. Some studies have analyzed the relative fitness of hybrids after interspecific crosses under laboratory conditions, and these studies have been successful in the characterization of postzygotic RIMs that keep species of plant pathogens apart at different phylogenetic scales (Table 1). These mechanisms are key in the persistence of species because they prevent nascent species from admixing (148, 151). Ceratocystis fimbriata sensu lato is a large complex of species that causes wild-type diseases of many economically important plants. Species within the group show strong specialization to cacao (C. fimbriata f. sp. cacaofunesta), sweet potato (C. fimbriata sensu stricto), and sycamore (C. fimbriata f. sp. platani ). Interspecific crosses between the different lineages show complex variation in reproductive isolation with high levels of phenotypic polymorphism. The results from these crosses can be categorized into three main types. The first type of cross produced no progeny (no perithecia were formed), indicating the existence of a prezygotic RIMs (or a very early postzygotic RIM). A second type produced perithecia with few ascospores, many of which were devoid of cytoplasm and showed deformed morphology. The colonies recovered from these ascospores were generally abnormal and showed restricted growth, indicating hybrid inviability at the ascospore level but also reduced fitness at the mycelial stage. The final type showed complete compatibility, indicating no intrinsic RIM between species (51). Similar variation in hybrid viability and fitness have been observed in conifer-specialized Ceratocystis (88), indicating that different Ceratocystis species show different types and degrees of reproductive isolation. It will be interesting to see whether the magnitude of reproductive isolation correlates with genetic divergence between species. 14.8

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These intrinsic mechanisms of reproductive isolation have also been characterized in oomycetes. In crosses involving divergent species of Phytophthora, only a very small proportion ( 1). This is a powerful approach but carries three major caveats. First, the identification of variants involved in habitat specialization is not equivalent with the identification of variants involved in speciation (e.g., if there is polymorphism and locally adapted populations within a population, dN/dS ratios might be significant, indicating positive selection without reproductive isolation). The second caveat is that dN/dS uses the number of synonymous substitutions as a proxy of neutral evolution and does not take into account codon bias (27, 144), thus underestimating the percentage of the genome under selection. Finally, and on a related note, dN/dS is a particularly conservative approach (111, 115, 197), and other approaches, such as modified McDonald-Kreitman’s tests, might be more informative (67, 100, 193).

Genetic Differentiation, Fst Fst (inbreeding coefficients as a proxy of population structure) is by far the most popular method to identify regions of the genome that are highly differentiated between populations or species. Calculating Fst values [or any of its analogs -ST , F ST , GST , θ, RST , (130, 195)] can be done using multiple approaches (97, 190) that are sensitive to particular demographic conditions (108). The premise of this approach is to compare variance components of phenotypic traits and try to determine whether there are molecular variants that are as differentiated as the phenotypes are. These comparisons can reveal what alleles are involved in divergent phenotypes (reviewed in 191). An expansion of this approach has been the study of populations that have had the chance to homogenize through gene flow (i.e., secondary contact of species in hybrid zones) in order to identify the genetic architecture of alleles involved in reproductive isolation. The identification of genomic islands of speciation (i.e., genomic clusters of sites with high Fst values) has at least three major caveats (28, 48, 134, 150). First, the calculation of Fst values is highly dependent on the quantification of genetic divergence within each of the species; if one of the species has a level of genetic polymorphisms that is much lower than the other, the average Fst value across the genome will be inflated. This might generate false positives. Second, regions with low genetic www.annualreviews.org • Speciation in Fungal and Oomycete Plant Pathogens


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Linkage disequilibrium: nonrandom association of alleles at two or more loci that descend from a single ancestral chromosome. Linkage disequilibrium does not require physical linkage

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diversity driven by positive selection will show high Fst values regardless of whether the genomic region is involved in reproductive isolation (134). Fst calculations between species are also heavily affected by retention of ancestral polymorphism, and deviations from the neutral allele frequency spectrum within species can lead to higher Fst values in regions of low recombination, even in the complete absence of interspecies gene flow (91, 92, 102, 103, 123, 161). Finally, when Fst values are calculated genome-wide, it is absolutely necessary to generate a background distribution in order to correct for false positives and the differential influences of recombination and selection. These violations might lead to the spurious detection of Fst outliers (3, 134).

Genetic Differentiation and Allele Frequency Differences An alternative quantification of divergence is the calculation of allele frequency differences across the whole genome (13). Even though this approach still requires the generation of an underlying background distribution to identify outliers, it does not suffer from the issue of differential levels of polymorphism within each species. Similarly, it does not depend on the influence of recombination and selection in different locations of the genome. An additional advantage of this approach is that it can be used in pooled-DNA sequences (109). Thus far, this approach has not been used in plant pathogens.

Candidate Gene Approaches Unlike other methods, this approach relies on previous knowledge generated in other organisms (reviewed in 125). This technique has been successful in identifying point alleles involved in a phenotype but does not reveal the whole genetic architecture of an adaptive trait (i.e., there is a negative ascertainment bias to discover alleles with small effect). An additional caveat is that for the identification of alleles involved in reproductive isolation, especially for phenotypes that cause intrinsic hybrid breakdown (i.e., sterility, inviability), there are no candidate genes to follow up, as hybrid breakdown can occur at many different biological levels.

Admixture Mapping For those pathogens that do not recombine in the laboratory but are thought to do so in nature, it is possible to sample areas in which two species with phenotypic differences overlap and hybridize (i.e., hybrid zones) and use linkage disequilibrium to map the genetic basis of traits. The premise of this approach is to use local ancestry estimates from each of the parental species and do association studies with particular phenotypes. Currently, there are several models that can be applied to identify admixture patterns in plant pathogens [HAPMIX (146), frappe (182), and ADMIXTURE (2) among others]. This approach has more power than common QTL approaches but has not been used in plant pathogens.

SPECIATION AND THE EMERGENCE OF NEW DISEASES Understanding the appearance of new pathogenic species can inform control methods and prevention plans (1, 181). Population genetics inferences and the study of evolutionary processes in fungi and oomycetes can reveal how pathogens emerge to cause new diseases. Emergence proceeds by one of three processes. The simplest scenario does not involve the evolution of new species and occurs when a pathogen colonizes a new geographical area in which it finds the host species that it infected in its ancestral location. Mycosphaerella fijiensis is an example of a recent worldwide 14.18

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epidemic that affects banana plantations. Molecular genealogies indicate that the range expansion of this pathogen has occurred through bottlenecks (i.e., severe population reductions) and that the spread of the disease might be caused by movement of plant material infected with ascospores (86, 155). A similar pattern is observed with the sudden oak death pathogen Phytophthora ramorum (82). This pathogen consists of several distinct genetic lineages that appear to have diverged a long time ago, possibly before modern agriculture (80). A second process of disease emergence occurs when a pathogen colonizes a new geographic area and develops the capability of infecting new hosts. This process, mediated by adaptation (via host shifts or expansion of the host range), enables the pathogen to thrive in hosts different from its ancestral plants. If the new adaptation leads to reproductive isolation from the parental species, then speciation is correlated to the emergence of the new pathogen and of the new pathogenic syndrome. Rhynchosporium, the causal agent of scald disease, seems to be composed of three cryptic pathogen species that have evolved by ecological divergence and host specialization to barley, rye, and Agropyron (198). Gene genealogies also suggest that Colletotrichum kahawae emerged as a pathogen that specializes in green coffee berries (173). The recent emergence of these pathogens is correlated with host shifts, suggesting that agriculture has played an important role in the emergence of diseases. A final possibility is that emergent pathogens and diseases originate after the hybridization between two species; the hybrid then shows a new suite of traits not observed in the parents (a type of inheritance known as transgressive segregation), allowing it to infect new hosts. Hybridization and admixture after bringing closely related pathogens into contact could favor cross-host-species disease transmission (71, 72). The demographic inference of gene exchange between plant-pathogen species in an explicitly spatial context can lead to a deeper understanding of the range constraints of plant-pathogen species.

CONCLUSIONS Evolutionary biology provides a powerful framework for understanding key aspects of the natural history of pathogens (114, 116, 196). The study of evolutionary processes in plant pathogens is a nascent field that promises to deliver new model systems and a comprehensive view of mechanisms involved in speciation and adaptation. On a more practical scale, the development of multilocus databases will allow for the identification of pathogenic lineages in a phylogeographic framework for additional comparative studies to understand the population dynamics of plant pathogens. One of the ultimate goals of plant pathology is to be able to predict the emergence of new pathogens, and this can be done using an evolutionary perspective. The combination of classical approaches coupled with high-resolution genomic studies will reveal demographic and genetic characteristics of how speciation occurs in oomycetes and fungal plant pathogens. The addition of new technological developments will bolster classical approaches and questions. Studying the evolutionary and ecological dynamics of plant pathogens can lead to a better understanding of how these organisms affect agricultural processes over time. The study of recently diverged pathogenic species can also address key questions in evolutionary theory. What is the level of gene flow required to override divergence by selection? What is the role of hybridization in the generation of more virulent pathogens? Do hybrids show new traits or do they always show reduced fitness compared with their parents? Does hybridization (and admixture) lead to the collapse of species boundaries? These questions, among others, are at the very core of evolutionary biology research but also have direct implications in the day-to-day management of plant diseases, as they essentially resolve the origins and mechanisms of emergence of new pathogens. www.annualreviews.org • Speciation in Fungal and Oomycete Plant Pathogens


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SUMMARY POINTS 1. Plant pathogens are an ideal system to study the evolution of reproductive isolation and how new species originate. The study of evolutionary processes in plant pathogens gives rise to new model systems and a comprehensive view of speciation and adaptation. 2. Although plant pathology research is usually not characterized as speciation-centered research, a series of studies have successfully identified the biological basis of reproductive isolation between plant-pathogen species. 3. The combination of classical approaches coupled with high-resolution genomic studies reveals demographic and genetic characteristics of how speciation proceeds in oomycetes and fungal plant pathogens. Annu. Rev. Phytopathol. 2014.52. Downloaded from www.annualreviews.org by College of William & Mary on 06/13/14. For personal use only.

4. The study of ecological and geographical drivers has important implications for plant pathologists and evolutionary biologists alike, and will lead to a better understanding of the events that lead to the emergence of new pathogens and new diseases. 5. The relative prevalence of speciation with versus without gene flow is still unknown for all taxa. Although speciation with gene flow might be possible in plant pathogens, it has not yet been proven. Geographical isolation can at least be assumed to play a role in most cases of speciation among these organisms.

FUTURE ISSUES 1. What levels of divergence are required to define species in fungi? Studies that connect molecular taxonomy with reproductive isolation are sorely needed. 2. The application of quantitative approaches to recognize species will reveal the existence of new plant-pathogen species. The application of these methods will allow for a global test of speciation and extinction rates within clades of plant pathogens. 3. Pathogen host range appears to be constrained by the pathogen effector repertoires. The interplay of effectors and plant immunity genes might shape the evolution of new plant-pathogen species. This hypothesis remains untested. 4. It remains unclear how frequently hybridization leads to host-range expansion. The formal study of the consequences of hybridization in plant pathogens is an open research avenue.

DISCLOSURE STATEMENT The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS We would like to thank K.L. Gordon, M.F. Przeworski, J.A. Coyne, P. Gladieux, J.W. Taylor, B.J. Knaus, and C.D. Cadena for scientific discussions and comments at every stage of the manuscript. 14.20

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S.R. and M.F.M. are funded by a Basic Sciences project from Facultad de Ciencias and Vicerrector´ıa de Investigaciones (Universidad de los Andes). D.R.M is funded by a Chicago Fellowship.


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