This document discusses speciation in fungi and oomycetes. It defines speciation as the evolutionary process by which new species arise. There are several mechanisms that can drive speciation, including allopatric, parapatric, peripatric and sympatric speciation. Reproductive isolation plays a key role in maintaining species boundaries and can occur through pre-zygotic and post-zygotic barriers. Genetic mechanisms like polyploidy can also cause reproductive isolation and lead to speciation. Speciation in plant pathogenic fungi may be driven by specialization to different host plants. Genome studies can help identify genes and regions involved in reproductive isolation and adaptation to new environments or hosts.

1. Akanksha Shukla
Ph.D. (Ag) 1st year
Dept. Of Plant Pathology

2. Fungi and oomycetes comprise a large number of species (Oomycota:
∼800 species; Fungi: ∼70,000 species)
Species- Species is a Latin word meaning ‘kind’. It is considered as a
fundamental unit of comparison in virtually all subfields of biology, from
anatomy to behaviour, development, ecology and evolution. It consists of
population(s) of organisms with similar features and monophyletic origin.
• The basic process of evolution recognizes the existence of two processes:
1. Anagenesis – phyletic change in the course of time. The species continue
to exist and survive as an interbreeding population
2. Cladogenesis or Speciation – the origin of new species of organisms
through splitting of pre-existing ones.

3. Speciation is the evolutionary process by which populations evolve to
become distinct species. The term ‘speciation’ was coined by (Cook 1906).
Speciation is the formation of new and distinct species in the course
of evolution. It involves the splitting of a single evolutionary lineage into
two or more genetically independent lineages, the process by which
biodiversity is generated.
Reproduction is regarded as one of the important species
differentiation factor. As organisms reproduce and genes replicate, changes
occur in populations thus accomplishing speciation (i.e. species change).

4. This concept was proposed by Linnaeus
In nature, there are limited number of types or universals and members of a
species form a class. It is also referred to as essentialism and the definition
of species based on this concept is also called essentialist species concept.
It is based on the degree of morphological differences used by the
taxonomists.
Under this concept, each species is entirely constant through time and thus
the concept does not allow any change in a particular species.
Since it is known that there are individual variations within the species and
different species may be morphologically identical as in the case of sibling
species (morphologically indistinguishable but reproductively isolated), the
essentialist species concept has been rejected

5. Occam and his followers rejected he idea of typological species concept and
for them only individuals existed and species had no real existence.
This species concept was popular in the 18th century.
Bessey (1908) suggested that nature produces only individuals and nothing
more. Species is merely a mental concept.
Species as a reproductive community of sexually and cross-fertilizing
individuals which share in a common gene pool. The members of a species
form a reproductive community, an ecological unit and a genetic unit.
These three properties (reproductive community, ecological and genetic
units) show that species cannot be defined by the typological or nominalstic
concepts. The biological species concept is the most widely accepted, but
there are three main difficulties in its application: insufficient information,
uniparental reproduction (hermaphroditism, automixis, parthenogenesis,
gynogenesis and vegetative reproduction) and evolutionary intermediacy.

6. Simpson (1961) proposed the evolutionary species concept and defined the
species as a lineage (an ancestral–descendent sequence of populations)
evolving separately from others and with its own unitary evolutionary role
and tendencies.
White (1978) has considered three main sets of variables which are involved
in the process of speciation:
i. genetic mechanisms generating genetic variability,
ii. genetic isolating mechanisms leading to the origin of reproductive
isolation, and
iii. geographic component

7. 1. Allopatric speciation-
Allopatric mode of speciation has also been called Geographic Speciation
During allopatric speciation, a population splits into two geographically
isolated populations. The isolated populations then undergo genotypic
or phenotypic divergence as:
(a) they become subjected to dissimilar selective pressures.
(b) they independently undergo genetic drift .
(c) These isolated populations undergo extensive genetic changes due to
the action of different evolutionary forces such as mutation,selection,
random genetic drift, migration and other factors and they genetically
diverge. When the populations come back into contact, they have evolved
such that they are reproductively isolated and are no longer capable of
exchanging genes and become independent species.

8. 2. Sympatric speciation –
Sympatric speciation is the formation of two or more descendant species
from a single ancestral species all occupying the same geographic location.
• Sympatric speciation involves instantaneous appearance of reproductive
isolation between the segments of the same population and new species
originate in the same geographical area.
• If one or both populations move out of the original habitat, two allopatric
species would be generated.
• If both the populations remain in the same geographical area, sympatric
species would be recognized.

9. 3. Parapatric-
In parapatric speciation, there is only partial separation of the zones of two
diverging populations afforded by geography; individuals of each species
may come in contact or cross habitats from time to time, but reduced
fitness of the heterozygote (Hybrid) leads to selection for behaviours or
mechanisms that prevent their interbreeding.
This process of improving allopatrically acquired isolating
mechanisms in a contact zone (a process corresponding to character
displacement) can be called parapatric speciation (Mayr, 1970)
4. Peripatric-
In peripatric speciation, a subform of allopatric speciation, new species are
formed in isolated, smaller peripheral populations that are prevented from
exchanging genes with the main population.

11. Reproductive isolation -The inability of a species to breed successfully
with related species due to geographical, behavioral, physiological, or
genetic barriers or differences.
The mechanisms of Reproductive isolation prevent members of
different species from producing offspring, or ensure that any offspring are
sterile. These barriers maintain the integrity of a species by reducing gene
flow between related species.
(In fungi having a long dikaryotic stage, nuclear fusion occur long after
individual or gamete fusion, which render the term post-zygotic
ambiguous. We shall therefore here use the term pre-mating and post
mating for fungi, which qualifies time before or after cell division)
1. Pre-Zygotic reproductive barriers
2. Post-Zygotic reproductive barriers

12. Pre-zygotic mechanisms
1. Temporal isolation- Individuals reproduce at different
times.
2. Mechanical isolation- Physical incompatibilities prevent
individuals from interbreeding.
3. Ecological isolation- Individuals live in different places
so they never meet up.
4. Behavioral isolation- Individuals ignore or do not get the
required cues for mating.
5. Gamete incompatibility- No fertilization occurs
Different species form and . .
.
Post-zygotic mechanisms
1. Hybrid inviability- Hybrid embryos die early, or new
individuals die before they can reproduce.
2. Hybrid sterility- Hybrid individuals or their offspring do
not make functional gametes.
Mating occurs and….
Zygote forms and….
Interbreeding is successful Reproductive isolation
mechanism
RIMs

13. Genetic Processes Include Some that Operate Only Within Species, and
Others that Function Between Species, Both Types maintaining Species
Cohesiveness.
BETWEEN SPECIES - vegetative incompatibility, Parasexuality are the avenue to
genetic exchange and recombination.
WITHIN SPECIES- Sexual compatibility systems regulated by mating-type genes
require two gametes with different mating-type specificities for a compatible mating.
Although mating types predate speciation events, mating-type genes evolve under
selection and are subject to recombination.
Eg: The mechanisms functioning between
species, intersterility in basidiomycetes, and general decrease in hybrid fitness
(well-demonstrated in the model systems, Neurospora and Saccharomyces) are of
direct interest as mechanisms of speciation.
.

14. This is a unique biological feature of fungi, with systems for self-signaling
in mycelial networks that explore and colonize, move nutrients, and make
direct contact with plants, animals, and other fungi. The opportunities for
horizontal gene transfer are there, but knowledge is rudimentary
The extent of asexual reproduction in fungi is exceptional. Extensive
asexual reproduction under selection could facilitate clonal speciation
relatively long-lived clonal lineages.

15. • Polyploidy and Aneuploidy are pathways to reproductive isolation and
speciation.
eg : Emerson and Wilson. (1954) made interspecies laboratory crosses of the
chytridiomycete Allomyces, which has alternation of haploid and diploid
thalli. The crosses produced a polyploid series in hybrids comparable to the
range in karyotypes observed among these species in the wild. There was a
drop in viability in the F1 (<5%), with a range of inviable results from
simple failure to germinate in the majority to production of aborted thalli.
In further crosses, however, meiospores of the F2 and F3 showed a striking
reversion to their parents’ level of high viability. An association between
viability and chromosome behavior was demonstrated.

16. These are dynamic, complex populations comprising subpopulations that
ariseand go extinct, drawing from at least one, relatively stable source
subpopulation.
Metapopulations may be important units in wild fungi, such as
ascomycetes with specific substrates or disturbance-mediated reproduction
(e.g., fire) and limited long-range dispersal.
In the most thorough investigation of the impact of metapopulation
structure (in the host) on coevolution, Burdon & Thrall have studied a
range of spatial and temporal scales in the Melampsora lini-Linum
marginale system with consideration of the implications for speciation in
the rust.
A key point in considering metapopulation structure as a route to speciation
is the potential for subpopulations to diverge through selection or drift,
potentially becoming reproductively isolated.

17. Dispersal may be long range or short range via meiospores or mitospores,
or through soilborne “spore banks” of melanized propagules, including
sclerotia, or through long-lived rhizomorphs or other mycelial aggregates
that migrate through substrate and soil from a colonized source.
Mechanisms of dispersal may be wind, water, insects, and larger animals,
including humans.
The outcome may be anything in the range from small discontinuous
populations, to large, spatially continuous individuals representing one
mitotic lineage. The type of dissemination has an impact on patterns of
allopatric speciation and on opportunities for sympatric speciation, most
likely by hybridization,

18. Saprotrophy, parasitic biotrophy, and mutualistic biotrophy will offer
opportunities for interaction among sympatric genotypes, or
alternatively isolate fungal species in very restricted niches, or
provide opportunities for parallel speciation.
Eg: Reinforcement of reproductive isolation among species of wood
decay fungi that may coexist as saprotrophs in the same log or patch
of soil. (Ullrich RC, Raper JR. 1975)

19. In fungi such as the Magnaporthe grisea species complex, it is
evident that lineage divergence is strongly associated with host
preference, both on the level of host species and host
variety/cultivar, and that there are important patterns in gains and
losses or losses in function of avirulence genes (Couch BC, Kohn
LM. 2002).
There is also evidence of a radiation in M. oryzae, evidenced by its
host range on grasses in all major groups, representing 10,000
species and some antiquity, compared with the relatively recent
origin of M. oryzae. With the elucidation of avirulence genes and
their evolutionary patterns, their role as mechanisms in speciation
should become clearer.

20. Fungal substrates or fungal species may be domesticated.
Eg : Forestry practice or construction with wood has had impacts, such
as creating an opportunity for hybridization or genetic drift through
a bottleneck that may be speciation mechanisms. The basidiomycete
Serpula lacrymans has split into two lineages, one associated with
wood in forests and one with structural wood. (Kauserud H, 2004).
Aspergillus oryzae was domesticated from an A. flavus ancestor
(Geiser DM., 1998,2000)

21. SPECIATION IN PLANT PATHOGENS
The completion of speciation is signaled by the existence of
distinct RIMs. A series of approaches has aimed at dissecting
the biological basis of reproductive isolation between plant-
pathogen species.
Classical studies
studies that have identified
RIMs between species
Genomic studies
involves genome-scale
studies that identify genomic
features that are involved in
reproductive isolation or in
interspecies differences

22. 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.
Eg 1) .Ascochyta (teleomorph Didymella)
Ascospores from Ascochyta fabae Ascospores from Ascochyta lentis
(disease in lentil but
not in fava beans)
(Disease in fava bean but
not in lentil)
Indicating strong host specificity and ecological isolation
This suggests a fitness depression in the hybrids and the presence of extrinsic
post zygotic isolation, and demonstrates an important role of environmental
factors in keeping these species apart
Hybrid produced fewer ascospores per ascus than pure species crosses,
indicating the existence of a post-mating non-ecological RIM.
No disease in either host

23. Eg. 2): Ceratocystis fimbriata sensu lato
Species within the group show strong specialization to -
cacao (C. fimbriata f. sp. cacaofunesta),
sweet potato (C. fimbriata sensu stricto),
sycamore (C. fimbriata f. sp. platani )
Interspecific crosses between the different lineages
Show complex variation in reproductive isolation with high levels of phenotypic
polymorphism
No progeny (no perithecia
were formed),
Indicating the existence of
prezygotic RIMs (or a very
early postzygotic RIM).
Perithecia with few with
deformed morphology
Complete
compatibility
Indicating no intrinsic
RIM between species
Indicating hybrid
inviability at the ascospore
level but also reduced
fitness at the mycelial
stage.

24. Genetic mapping of traits using crosses or genome-wide association
studies enables discovery of adaptive traits, including those involved in
reproductive isolation. These approaches have been used in Cochliobolus
sativus (Zhong et al., 2002), Fusarium graminearum (teleomorph:
Gibberella zeae) (Gale et al., 2005), Magnaporthe spp. (Chuma et al.,
2011), and Stagonospora nodorum (Friesenetal.,2012) among others. This
has resulted in identification of genes conferring virulence and the
evolutionary processes that lead to their evolution.
Genome-wide data can also be used to identify regions that have undergone
a large influence of natural selection in the adaptation to new environments
and might thus be involved in habitat isolation Gene scans for regions that
have evolved under the influence of natural selection have identified a set
of genes in M. graminicola that show strong signatures of positive
selection (fast rate of amino acid substitutions) (Stukenbrock et al ., 2010).

25. Three possible scenarios in which reproductive isolation arises are shown. Each color
represents a different species.
(a) Geographical factors
lead to the accumulation
of genetic differences
and the buildup of
reproductive
isolation.
(b) Environmental
factors, such as host
or temperature, can
lead to reproductive
isolation over time.
(c) In some rare instances, hybrid
individuals might be reproductively
isolated from the parental species
while still being fertile. In these
cases, collectively referred as hybrid
speciation, speciation does not occur
through divergence but instead
occurs through reticulation.

26. Source: Restrepo, S., Tabima, J. F. (2014)

27. Understanding Population genetics
inferences and the study of evolutionary
processes in fungi and oomycetes can
reveal how pathogens emerge to cause
new diseases and inform about the
prevention plan. Emergence proceeds by
one of three processes.
It 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 epidemic that affects
banana plantations
It occurs when a pathogen colonizes a new
geographic area and develops the capability
of infecting new hosts. This process,
mediated by adaptation , enables the
pathogen to thrive in hosts different from
its ancestral plants. 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
It occurs when 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

29. The word Pleomorphism is of Greek origin- pléō, "more" and morphḗ, form. It
is the ability of the Fungi to alter their morphology, biological functions or
reproductive modes in response to environmental conditions.
Telomorph-
The sexual state of a fungus (the state in which two fungal nuclei unite and
undergo meiosis, forming offspring with new genetic information). Fungi t
hat have teleomorphic states are said to be “perfect” fungi.
Anamorph-
A somatic or reproductive structure that originates without nuclear
recombination (asexual reproduction); the imperfect part of the life cycle of
fungi.
Synanamorphs-
When a single fungus produces multiple morphologically distinct
anamorphs. Eg . Hypocrea
Holomorph-
the whole fungus, including anamorphs and teleomorph iscalled
Holomorph.

30. Pleomorphism is one of the greatest challenges of systematic mycology.
Holomorphic fungi that are known to produce both sexual and asexual
spores have caused difficulties for the taxonomists attempting to place them
within classifications.
Fungi are classified primarily based on the structures associated
with sexual reproduction, which tend to be evolutionarily conserved.
However, many fungi reproduce only asexually, and cannot easily be
classified based on sexual characteristics; some produce both asexual and
sexual states. These problematic species are often members of
the Ascomycota, but a few of them belong to the Basidiomycota.
Even among fungi that reproduce both sexually and asexually, often only
one method of reproduction can be observed at a specific point in time or
under specific conditions. Additionally, fungi typically grow in mixed
colonies and sporulate amongst each other. These facts have made it very
difficult to link the various states of the same fungus.
Fungi that are not known to produce a teleomorph were historically placed
into an artificial hylum, the “Deuteromycota," also known as “fungi
imperfecti,".

31. The New Situation
The International Botanical Congress in Melbourne in July 2011 made a
change in the International Code of Nomenclature for algae, fungi, and
plants and adopted the principle "one fungus, one name".
The separate nomenclatural status afforded to anamorph-typified and
teleomorph-typified names ended on 30 July 2011. Regardless of the life-
history state represented by their types, all legitimate fungal names are now
treated equally for the purposes of establishing priority. The special rules
permiting dual nomenclature no longer apply.
In some instances, generic names with type species typified by an anamorphic
state, and names of genera, species, and infraspecific taxa with anamorphic
name-bearing types, will have priority over currently used teleomorph-
typified names.

32. Evolutionary biology provides a powerful framework for understanding
key aspects of the natural history of pathogens. 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.
The combination of classical approaches and high-resolution genomic
studies will reveal demographic and genetic characteristics of how
speciation occurs in oomycetes and fungal 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.

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