What is a fungal species?
Species
• Are species real?
• How do we define a species?
• Is there one “right” species concept that will
be applicable to all organisms?
• What is the difference between a theoretical
species concept and a operational species
concept?
Species—Latin, kind
• A species is the principal unit of evolution
(Ernst Mayr 1980)
• The lowest principal rank in the nomenclatural
hierarchy (Dictionary of the Fungi)
Theoretical species concept
• Evolutionary Species Concept (Simpson 1951,
1961; Wiley 1978)—A single lineage of ancestordescendent populations which maintains its
identity from other such lineages and which
has its own evolutionary tendencies and
historical fate.
Operational Species Concepts
• Morphological Species Concept
• Biological Species Concept
• Phylogenetic Species Concept
Morphological Species Concept (MSC)
• Traditional approach in mycology—species are
units that can be delimited on the basis of
morphological characters, ideally by
discontinuities in several such characters.
Example
• Ceuthospora lunata, a coelomycete causing
black rot disease of cultivated cranberry in
eastern North America
• “light” and “dark” strains recognized based on
colony morphology
• Cranberry fruit inoculated with dark strain
developed a uniform black rot, fruit inoculated
with light strain developed a pale brown
discoloration
Dark strain conidia
7-15 x 2-3.5 μm
Light strain conidia
6-11 x 2-3.5 μm
Strasseria geniculata –
another fruit rot pathogen
Conidia
• Light strain = Allantophomopsis cytisporea,
originally described by Fries (1893) on
Vaccinium vitis-idaea in Sweden
• Dark strain = Allantophomopsis lycopodina,
originally described by von Höhnel (1909) on
Lycopodium in Austria
Carris (1990) Can. J. Bot. 68:2283-2291
Biological Species Concept (BSC)
• Species are groups of actually or potentially
interbreeding natural populations, which are
reproductively isolated from other such
groups (Ernst Mayr 1942)
Tilletia L.-R. & C. Tulasne 1847
• Type species: Tilletia caries
(DC.) Tulasne based on 1815
specimen from Triticum
aestivum (France)
• T. laevis Kühn (1873) based on
1872 specimen from wheat
(Germany)
Short or dwarf bunt of wheat
• First published report from
Montana in 1935:
– Stunted plants
– Spore balls (sori) hard,
compact and round
– Spores do not germinate
under same conditions as T.
caries and T. laevis
– Soil infestation is the main
source of infection; seed
treatments ineffective
Common bunt teliospores
Dwarf bunt teliospores
Tilletia contraversa Kühn (1874)
• Based on smut in ovaries of
Elymus repens from Germany
– Kühn compared quack grass
smut with wheat bunt based
on spore morphology and
germination
Dwarf Bunt or TCK Smut
– Reticulate teliospores with
gelatinous sheath
– Germination in 3-6+ wk at
3-8 C; requires light (T.
caries & T. laevis germinate
in <7 da at 15C without
light)
– Dwarf bunt infection occurs
with deep, persistent snow
cover
– Dwarf bunt pathogen
considered to have a wide
host range including 45
grass species in 17 different
genera
Species
Spores
Germination
# Sporidia
T. caries
Reticulate
Exospore < 1 μm
14-25 μm diam
1-2 wk at 15C
light or dark
4-16
T. laevis
Smooth
14-22 μm diam
1-2 wk at 15C
Light or dark
4-16
T. contraversa
Reticulate with gelatinous
sheath up to 5 μm thick
Exospore > 1 μm
17-27 μm diam
3-10 wk at 5C
Light required
14-30
The wheat bunt species are reproductively
compatible
• Putative hybrids with spores exhibiting
intermediate morphology found in natural
populations
• Experimental hybrids generated by coinoculation of wheat:
– T. caries x T. contraversa
– T. caries x T. laevis
Russell & Mills. 1993. Electrophoretic karyotypes of Tilletia caries, T. controversa, and their
F1 progeny: further evidence for conspecific status. MPMI 6:66-74
Questions
1. If T. caries, T. contraversa and T. laevis are
reproductively compatible and produce
viable progeny, should they be recognized as
one, two, or three species?
2. Is additional evidence needed? If so, what
type of evidence?
MP analysis-- EF1A, ITS, RPB2
70
T. caries 4
T. caries J19
T. laevis 98-194
Germination at 5C
T. laevis V766
Triticum spp.
T. contraversa WSP 71280
87
94
T. contraversa V528
T. contraversa 94-10
T. laevis WSP 71278
100
100
T. trabutii V764
Hordeum spp.
T. trabutii VPRI 32106
T. secalis WSP 71279 Secale cereale
99
100
83
T. brevifaciens HUV 20.802
Thinopyrum intermedium
T. brevifaciens V412
T. bromi ChInterc LC1328
T. bromi WSP 71272
T. bromi WSP 71273
84
82
100
90
99
100
T. vankyi WSP 71266
Lolium perenne
T. vankyi ChInterc LC1326
T. vankyi ChInterc LC1325
Festuca rubra
T. vankyi WSP 71270
T. vankyi FF7-8
93
100
100
Bromus spp.
T. bromi WSP 71271
100
100
86
87
T. laguri HUV 16.352
Lagurus ovatus
T. lolii V767
Lolium rigidum
T. goloskokovii WSP 71281
Apera interrupta
T. goloskokovii WSP 69687
T. goloskokovii WSP 69688
100
100
T. sphaerococca ChInterc LC1327
T. lolioli V763
Agrostis stolonifera
Loliolum subulatum
T. fusca WSP 71275
Vulpia microstachys
T. elymi WSP 71274
100
100
5 changes
T. togwateei WSP 71277
T. togwateei WSP 71276
Poa reflexa
Elymus glaucus
Pimentel et al. 2000. Characterization of interspecific hybrids
between Tilletia contraversa and T. bromi. Mycologia 92:411-420
• Has reproductive compatibility been retained
among host specific species of Tilletia?
– T. bromi and T. contraversa are closely related
species with overlapping host range; sympatric
populations common in wheat fields in PNW
Pimentel et al. 2000. Characterization of interspecific hybrids
between Tilletia contraversa and T. bromi. Mycologia 92:411-420
Questions
1. What can you conclude from the Pimentel et
al study regarding reproductive compatibility
of T. bromi, T. contraversa, and T. laevis?
2. Do the results of this study provide evidence
for or against the conspecific status of the
wheat bunt pathogens?
Phylogenetic Species Concept (PSC)
• A species is the smallest (exclusive)
monophyletic group of common ancestry (de
Queiroz & Donoghue 1988)
Example: Morchella
• Morchella –true morels
– Black morels—M. elata group
– Common morels—M. esculenta
– Half-free morels—M. semilibera
Morchella elata group--Black Morel
Morchella esculenta—
Common or Yellow Morel
Morchella semilibera—Half-free morel
Morchella esculenta courtesy of
George Barron
Mountain BlondeVerpa
Morel—undescribed
species
conica
Verpa bohemica
Summary
• 3 major clades corresponding to black morels
(24 species), yellow morels (16 species), and
M. rufobrunnea
• 37/41 spp with Laurasian distribution with 33
spp represented by multiple specimens
exhibiting continental endemism:
– 16/18 North American
– 13/15 Eurasian
Limitations to MSC
• Fungi have a limited number of morphological
traits, these traits can be highly plastic
– Pleomorphy, dimorphism
– Intraspecific morphological variability
• Morphological traits may evolve slowly and
recently diverged species may not differ
morphologically
Limitations to BSC
• 20% of fungi are asexual, others are
homothallic or can’t be grown or crossed in
artificial culture
• Interbreeding may be retained as an ancestral
trait
Limitations to PSC
• Distinguishing populations from species-where to draw the line
• Genealogies of different genes may give
different species
– Introgression, hybridization and horizontal gene
transfer
• Recently diverged lineages may not show
reciprocal monophyly
Genealogical Concordance Phylogenetic Species
Recognition (GCPSR; Taylor et al 2000)
• Based on concordance of multiple gene
genealogies:
– Is the clade present in the majority of single-locus
genealogies?
– Is the clade well supported in at least one singlelocus genealogy?
– Is there support for the clade in the combined
gene tree?
Fig. 3 from Taylor et al. 2000
Species concepts vs. speciation
• Species are separately evolving
metapopulation lineages that acquire
properties (reproductive isolation, ecological
and phenotypic differences) at different time
points during the course of divergence (de
Queiroz 2007)
de Queiroz K PNAS 2005;102:6600-6607
A unified species concept?
• “Lineages do not have to be phenetically
distinguishable, diagnosable, monophyletic,
intrinsically reproductively isolated,
ecologically divergent, or anything else to be
considered species. They only have to be
evolving separately from other lineages.” (de
Queiroz 2007)
Another unified species concept
• “A species is the smallest aggregation of
populations with a common lineage that share
unique, diagnosable phenotypic characters.”
(Harrington & Rizzo 1999)
Consolidated Species Concept
• Extension of the “polyphasic” approach to
fungal identification that weights MSC, ESC
and PSC characteristics (Quaedvlieg et al 2014.
Persoonia in press)