MODULADVANCED MICROBIOLOGY

FUNGAL SPECIATION

by

Gayuh Rahayu

Microbiology Study ProgramDepartment of Biology

Faculty of Mathematic and Natural SciencesBogor Agricultural University

2010

INTRODUCTION

Speciation of fungi has not been explored deeply, though in fact fungi are simpleorganisms, that easily to manipulate in the lab, with a short generation of times, flexibilityof response to the environmental change, often haploid-genetic based. In this chapter,components that contribute and determine the fungal speciation under the classical theoryof speciation is explored. There are two kinds of speciation processes which differ intheir sequence of events and factors determine the type of speciation (Fig 1) i.e. sympatricand allopatric speciation. The kinds of speciation occurs in fungi may depend on thedispersal modes of the fungal propaguls. The dispersal mode will overecome the

geographical barrier, for instances Puccinia graminis which have dry and lighturediniospores may distribute towards the north America continent within 2 monthspassing over all the valley and mountain (Fig 2).

A. Single population with homogenousenvironment

B.

C.

Differentiation of environment and

migration to new environment producedifferentiation of races and subspecies

Further differentiation and migrationproduces geographic isolation of some

races and subspecies.

D. Isolated subspecies differentiate withrespect to their genome that controlreproductive isolation

Fig. 1. Sequence of events for speciation

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Original morphospecies Subgroups (biological species) Postulatedspeciation

aprocess

Degree ofreproductive

bisolationBasidiomycetes :Armillaria mellea

Auricularia auricula

Coprinus macrorhizus

Rizoctonia solani

Puccinia graminis

Europe (5)N America (>10)

European vs N AmericanN American deciduous vsconiferous

Two intersteril groups

11 anastomosis groups withinThanateporus cucumeris orCeratobasidiium cornigerum

f.sp. tritici, f.sp. secalis, f.spavenae and f.sp. recondita

EE

GEH

SU

SU

EH

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Fig 2. Northward spread of black rust on wheat as a result of urediniospore dispersal byair current

DEFINITION AND ELEMENTS OF SPECIATION

Speciation is defined as the emergence of reproductively isolated sub-population from orwithin an original interbreeding population or evolution of a species. To understand thethis definition, we have to firstly understand the principal of population and isolation. Theemergence of sub-populations will often be associated with accumulation of geneticdifferences, which may not be always expressed in morphology. Speciation is not alwaysrelated with the concept of morphological species, but closer to biological species.

Tabel 1. Subgroups within fungal morphospecies and their status

Ascomycetes and fungiimperfecti

Erisyphe graminis

Pyricularia oryzae

Seven forma specialis

Types I-III

EH

EH

-

Chytridiomycetes

Coelomyces dodgei

C. dodgei and C. punctatus E

Zygomycetes

Mucor hiemalis

M. hiemalis, M. corticola, M.lausanniensis, M. luteus, M.sylvaticus

E

Oomycetes

Phytophthora palmivora

Cacao and rubber forms EH -

Myxomycetes

Didymium iridis

Heterothallic and non heterothallicgroups

E

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a) G = geographical speciation; E = sympatric speciation in response to ecological influence, EH where Ecaused by host specialization, SU, probably sympatric and no apparent cause

b) = total; = partial; - = no information

Expression im morphology developed long after the initial speciation occured andreproductive isolation may sometimes instantenous. Therefore, we often find in thelitterature, many examples of fungal morphospecies within which there are partially ortotally reproductive isolated sub-groups (Tabel 1).

There are four elements contributing to speciation i.e. the original interbreedingpopulation, the genetic system, natural selection and reproductive isolation. How theseelements apply to fungi will be explained.

Original Interbreeding Population and Its Genetic System

A population can be defined in terms of numerical size, geographic size, and geneticstructure. The geographic size maight be local or cosmopolitan depends on the mode anddispersal range of propaguls, the size and distribution of the subtratum and of ecologicalniche occupied. Even freely interbreeding cosmopolitan species such as Schizophyllumcommune may be partially fragmented into smaller locally adapted units. In this speciesgene flow mostly local, but gene flow from distal range is sufficient to preserve thegenetic integrity.

Understanding the genetic structure of a popiulation is important to elucidate speciationphenomena. Most local samples of regularly outcrossing Ascomycetes, Basidiomycetesand Myxomycetes contain large number of individual genotypes and often represented asa vegetatively incompatible individuals. This kind of groups often occur in relativelyundisturbed environment. For example, Ophiostoma ulmi (Fig. 3) contains many

selection, none of those selection components varies so strongly that longer termecological balance is disturbed. Thus, routine selection favours maintenance of a stablepopulation structure. In contrast, episodic selection results from any form of sudden andextreme ecological disturbance leading to breakdown basal population structure. Theeffect of episodic selection can be directional with respect to certain traits in the fungalpopulation.

The routine and stabilizing selection process on a population can be examplified byexperiment on S. commune (Fig. 4). A local samples of 77 dikaryons was found to beheterogenous for growth rates, fruiting characters mating types and vegetativecompatibility types and can be considered as a basal population structure. When two

dikaryons near the extremes of growth rate variation were individually fruited and

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vegetative incompatible groups that maintain their integrity of the individuals bypromotion of antagonism or invasion between them.

Fig. 3 Population of (more than40 vc groups) Ophiostomaulmi on 11 x 16 cm wood

of elm tree

The structure of the basal population of fungi may also diffrentiate by isozymepolimorphisms as in Neurospora intermedia and Dydimium sp., by mating-type factorsas in Coriolus versicolor, growth rate and ability to fruit as in S. Commune. In the termof basal population structure, the population is a highly heterogenous local populationstructure within which regular outcrossing and vegetative incompatibility play a majorrole. There are two important points in the speciation. Firstly, speciation occurs in thisbasal population and moderate to strong distortions may initiate speciation. Secondly, forasexual fungi, natural selection will operate in the individual or gene level.

Natural Selection

Natural selection acts on basal population via many aspects and during many stages oflife cycle; e.g. via the substrates or hosts, vectors, climates, competitors, during sporegermination, colonisation, consolidation, fruiting, dispersal and resting stages. Theselection mode can be divided into two i.e. routine and episodic selection. In the routine

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inbred. The two reulting set of 72 dikaryons showed much greater variation than its basalpopulation. This indicated the impact of selection on a single field generation.

Natural Selection by Gradual Niche Divergence and Desruptive Selection

When a basal population confronted with two or more ecological niche, a gradual shiftwill occur as a result of disruptive selection. Climate, living and non-living substrats arefactors promote divergence. For example, Typhula ishikariensis (snow moulds) consistsof three biotypes, A, B and C. Biotype A occur mainly in inland with deeper and longersnow cover, whilst biotype B distributed in coastal region. Those two biotypes arereproductively isolated. Biotype C is similar to B but irregular in distribution. Biotype Aand B may have gone into complete speciation.

Opportunistic nutritional strategies often lead to divergence among saprotrophs.Examples are Mucor and Neurospora. M. mucedo commonly inhabites rodent dungwhilst the morphology similar to M. pyriformis which is common in rotten fruits. In N.Intermedia, there are two subpopulations ‘yellow giant’ occuring on food and in foodwaste in east and south east Asia, and ‘standard’ occuring on burned subtrate in thetropics. Individuals from the two populations will hybridise but the hybrids probably donot survive in nature.

Host defence mechanisms influence the divergence among the plant pathogens.Divergence of population in response to narrow host niches depict by occurance of

= Wild dikaryons

= Synthetic dikaryons

Growth rate (mm/10 da)

Numberof

Isolates

Fig. 4. The routine and stabilizing selection process on a population can beexamplified by S. commune

partially or totally reproductively isolated forma specialis of powdery mildew (Erysiphegraminis) and rust (Puccinia graminis) in different genera of cereal and grasses. Abroader niche specialisation represented reproductive isolation is ‘pine’ and ‘spurce’ form

of Heterobasidion annosum. The other example is ‘deciduous’ and ‘coniferous’Auricularia auricula.

Reproductive isolated subgroups exhibiting spectrum of host can be found within a singlemorphospecies, as in Giberella fujikuroi and Nectria haematococca. Giberella fujikuroigroup A exists on corn, cotton pine, and sorghum, group B on corn, pine and sugarcane,group C on rice, and group D on corn, pine, sugarcane, copra, Cymbidium and, Hibiscus.N. haematococca can be divided into 6 mating population (MP), MPI on cucurbits, MP IIon potato, MP III on mulberry, MP IV on Japanese pepper. MP V on cucurbits and MPVI on pea, mulberry, ginseng and chick pea. Each MP is heterothallic and reproductivelyisolated. Homothallic forms also exist, but are saprophytic. MPVI might be an ancestralform, a less specialized population adapting to a wider host range and freelyinterbreeding. A specialized genetic system is needed to confer a higher level ofadaptation to a particular host.

Pathogens with a wide host range might have been exists before man’s disturbance andcultivation of their host which caused the pathogens to be more specialized. This isshowed by the result of the experiment of E. graminis and P. graminis, where hybridsbetween certain forma speciales have wider graminaceous host range but less pathogenicon the individual host than its parents. Further E. graminis from wild grass communitiesin Israel have a wider host range than isolates from elsewhere.

Division of living and non-living substrate in sympatric speciation is shown byLophodermium on pine. Lophodermium can be divided into three physiological species,one infect green needles i.e parasitic, one occurs on killed needles and the other onneedles litter.

A large number of fungal morphospecies in Basidiomyctes which contain reproductivelyisolated sub-groups has no evidence of niche relationship. For example, intersterileanastomosis groups within Thanatheporus cucumeris and Ceratobasidium conigerum.This could be that they were originally a product of allopatric speciation, but maninfluence brought them into one ecological niche. For example, intersterile gropus ofSistronema brinkmanii occurs on the same wood piece.

Reproductive Isolation

Classic speciation theory requires that some forms of reproductive isolation strengthens,sustains and in some cases promotes the divergence of an originally interbreedingpopulation into sub-populations. The reproductive isolation can be divided intogeographic isolation, pre and post zygotic. Geographical isolation worked on primaryspeciation. While pre and post zygotic worked on a population in the same geographicallocation in gradual ecological niche.

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In pre-zygotic isolation, if the majority of fertilizations are local, the habitats (ecologicalisolation) may tend to isolate the sub-populations. However, the pre-zygotic isolationmight also be due to gametic isolation. The gametic isolation worked on gametes release(temporal isolation), prior to plasmogamy (behavior isolation) or work on post contactphase (post contact isolation). Temporal isolation was shown by Coelomyces dodgei andC. punctatus which release their gametes in the different periods of time. In the behaviorisolation, plasmogamy is often preceded by chemically mediated growth and recognitionprocess such as in interactive zygophore development in Zygomycetes, hormonallyregulated gametangial development in Oomycetes. Their breakdown would lead toreproductive isolation. Post-contact isolation involves a breakdown of the next step in thefungal mating: fusion of gametangia or hypha.

In the post zygotic isolation, the process of isolation might occur due to zygotic abortionor genetic disharmony or hybrid sterility. The zygotic abortion includes meiotic failure inin haploid based system and failure of oospores formation. Chromosomes differencesbecome the major factor as in P. megakarya and P. palmivora which occur in cacaoplantation in West Africa. These species differ in the chromosome number and size. Thetwo species can mate, but gametangia of the hybrid are unable to produce oospores.Genetic disharmony produced defective ascospores, and the germling lack vigor,reflecting genetic disturbances or germlings are vigor but unable to survive. In hybridsterility, hybrid F1 progeny in nature may survive, but be sexually sterile. For example,the hybrid meiospores of C. dodgei >< C. punctatus crosses are motile and able toencyst, but fail to grow further to their somatic phase. The sterile diploid form ofPhythopthora meadii is probably another example.

Questions:

1. If we found P. capsici on pepper in Bangka and P. capsici on chili in India.

Give a hypothetical speciation that might occur in that species.

2. Explain briefly any possibility of geographical isolation for Puccinia graminis.

3. If we found hybrid of P. meadii as a progeny of crossing between P. palmivora andPhytopthora indigenous on rubber SriLanka and India. P. meadii is a diploid form.What barrier works on P. meadii that making P. palmivora and Phytopthoraindigenous be treated as different species.

References:

Brasier CM. 1987. The dynamic of fungal speciation. In Rayner ADM, CM Brasier andD. Moore (eds) Evolutionary Biology of the Fungi. Cambridge: CambridgeUniversity Press. p. 231-261