New
Review
Phytologist
review
Research
and
trysts,
genomicmergers,
Cryptic
plantspeciation
F.Wendel2
RichardCronn1andJonathan
Authorforcorrespondence:
JonathanF Wendel
Tel: 515 294 7172
Fax: 515 294 1337
Email:jfwviastate.edu
Oregon
Way,Corvallis,
3200 SW Jefferson
USDA ForestService,
Station,
Research
'PacificNorthwest
Ames,
IowaStateUniversity,
Biology,
andOrganismal
ofEcology,
Evolution,
97331USA; 2Department
Iowa50011 USA
Received:28 July2003
Accepted:26 September2003
doi:10.1046/j.1469-8137.2003.00947.x
Summary
speciation,
Keywords:hybridization,
geneflow,Gossypium.
introgression,
It has longbeen recognized
thatinterspecific
hybridization
is commonin plants,
ofdiversification
andspeciation.
Withthewidespread
utilizaenhancing
processes
- as revealedthrough
tionof molecular
tools,interspecific
hybridization
incongruto be evenmore
enceamongtwoormorephylogenetic
datasets- isnowinferred
prevalent
thanindicated
bymorphological
andcytogenetic
evidence.UsingGossypiumas an example,we showhowmultiple
molecular
markers
haveimplicated
a
highfrequency
ofhistorical
hybridization
betweenlineages
whosemodern
descendantsarestrongly
isolatedbygeography
andintrinsic
Forexample,
geneticbarriers.
transoceanic
ofpropagules
Africa
to theNewWorldledto thecreadispersal
from
tionofa novelallotetraploid
as wellas theintrogression
ofAfrican
lineage,
repetitive
elements
intoa Mexicandiploidspecies.Bymechanisms
thatremain
obscure,
fully
of modernGossypium
historical
one-quarter
speciesappearto haveexperienced
interspecific
cytoplasmic
and possiblynuclearintrogression.
These remarkable
observations
ofinterspecific
a genusforwhichsuch
geneticexchangeemergefrom
contactwouldappearimprobable,
is a more
implying
thathistorical
hybridization
inangiosperm
creative
forcethansuspected
evolution.
? NewPhytologist
(2003) 161: 133-142
Introduction
In his 1981 classic, Plant Speciation,Verne Grant (1981)
devoted six chapters and 88 pages to the subject of
interspecific
hybridization.
Comprisingmore than a fifthof
the volume, this separatelydemarcated section, entitled
Naturalhybridization
and itsproducts,
of
provideda synthesis
our understanding
oftheprevalenceofhybridization
in plants
and the spectrumof possible evolutionaryoutcomes.This
treatment,
offeredover20 yrago, testifies
to a long-standing
? NewPytologist(2003)
161:133-142
www.newphytologist.org
recognitionamong botanistsof the high frequencyand
evolutionarysignificanceof interspecificcontact among
plants.Of course,mostof the evidencethatGrantused and
citedwas morphological,
althoughinsightsalso emergedfrom
cytogeneticand geneticinvestigations.
For example,Grant
noted thatinterspecific
hybridsof Opuntiaspinosior
and 0.
versicolor
(Grant& Grant,1971) and Aquilegiaformosa
x A.
pubescens
(Grant,1952) displayeda patternof morphological
intermediacythat was straightforward
to interpret.LeafystemmedGilia species,however,presenteda more complex
133
134
Review
review
Research
New
Phytologist
isolatedfromone another,
hasnot
Gossypium
patternthatposed a substantial
challengeto traditional geographically
ofhybridization
has
classification
approaches(Grant,1953). Elucidatingthe beena groupforwhicha highfrequency
havebeenusedtoargue
Indeed,thesehurdles
a synthesis
of beensuspected.
ofthereticulating
Giliacomplex
origin
required
thatreticulate
evolutionamongdiploidcottonspeciesis
information
derivedfrommorphometric
(Grant,1950;
unlikelyand unimportant
(Fryxell,
1971; Fryxell,
1979).
Grant,1953),cytogenetic
(Grant,1953; Grant,1965),and
molecular
studies
arrive
phylogenetic
frequently
transmission
geneticstudies(Grant,1966).Theseexamples Nonetheless,
thatinterspecific
namely,
hybridthatplantlineagesmaycomprise at theoppositeconclusion,
and othersdemonstrated
in
and important
widespread
reticulatenetworksratherthan exclusively
bifurcating izationhasbeenexceptionally
it appearsthatsome
of thegenus.Moreover,
theevolution
independent
entities.
suiteof
eventsinvolvespecieswhosepresent
toolsover hybridization
ofmolecular
The advent
andapplication
genetic
features,
biogeography,
andintersterility
posesuch
thisfeature
ofplantevo- life-history
thelastdecadesnotonlyconfirmed
thatthe
isolation
barriers
preandpost-reproductive
lution,butalso enormously
expandedthelistofplanttaxa striking
ofsuccessful
mergers
wouldseemto be nil.Here,
ofrecent
orhistorical likelihood
thatappeartohaveexperienced
episodes
and
the evidenceforthese'cryptictrysts'
introgression.
Molecularinvestigations
havebeenextraordi- we summarize
evolution,drawing
in confirming
thehybridnatureofmany 'genomicmergers'duringGossypium
narilysuccessful
species(Arnold,1997;Rieseberg,
1997) andhavepermitted attentionto insightsthathave emergedfromcombined
molecularandmultiple
characterization
of thesize and shapeof contact genetic,
cytogenetic,
biogeographic,
fine-scale
is thatsince
Our perspective
basedinvestigations.
zones(Rieseberg
&Wendel,1993;Arnold,
1997).Anincreasinglymarker
exhibits
traits
anddiscommonobservation
in molecularphylogenetic
unremarkable
studiesis
Gossypium
reproductive
theevolutionary
of interspecific
incongruence
amongtreesderivedfromindependent
cyto- persalbiology,
significance
is probably
evengreater
thanthatenvisioned
plasmic(e.g.chloroplast
[cp]DNA) andnuclear(e.g.riboso- hybridization
Thispattern
ofincongruence notonlybyGrant(1953,1981)butbycontemporary
authors
malDNA) molecular
markers.
numerous
causes(Wendel& Doyle,1998),but (Arnold,
mayreflect
1997;Rieseberg,
1997)as well.
the biologically
mostnoteworthy
is 'cryptic'interspecific
andintrogression
hybridization
(Rieseberg,
1997;Wendel&
inGossypium
Evidence
forcryptic
hybridization
markers
Doyle,1998;Raymond
molecular
etaL,2002),whereby
transferred
dueto interspecific
contradic- Gossypium
geneflowgenerate
includesabout 50 species (Fryxell,1992),
inferences.
including
18 speciesnativetotheNewWorld,12-14 species
toryphylogenetic
To date,onlya fraction
ofplantgenera
havebeensubjected nativeto Africa/Asia,
and 18 speciesnativeto Australia.
to molecular
thathaveemployed Relationships
withinthe cottongenushavebeen inferred
phylogenetic
investigations
thatpermitthe usingmorphology
molecularmarkers
multipleindependent
(Fryxell,
1971;Fryxell,
1992),interfertility
detectionof interspecific
and cytology(Endrizzietal., 1985) and
geneflow.Despitethisshallow relationships
oftaxaandmolecular
thenumber
ofcases molecular
sampling
markers.
area wealthofgenetic
markers,
Amongthelatter
of inferred
historicalhybridization
eventsis remarkably data,including
sitevariation
cpDNA restriction
(Wendel&
& Soltis,1991; Rieseberg,
high(Rieseberg
1991; Wendel Albert,1992), DNA sequencevariationfromchloroplast
etaL, 1991;WendeletaL, 1995b;Wendel& Doyle,1998).
genes(Seelananetal., 1997;Smalletal., 1998;Cronnetal.,
theseobservations
thatinterspecific
Together
suggest
hybrid- 2002), DNA sequencevariationfromnuclearribosomal
izationmaybe a morepowerful
and creative
evolutionary DNA (5S geneandspacer,
Cronnetat., 1996,5.8S geneand
thanenvisioned
process
bytheearlyproponents
ofhybridiza- flanking
internal
transcribed
Seelananetal., 1997),
spacers,
tion,suchas Grant(1981),Anderson
from10 low-copy
(1949) and Stebbins andDNA sequences
nucleargenes(Small
oneremarkable
(1950).Moreover,
aspectofthemanyrevela- etal., 1998;Seelananetal., 1999;Small& Wendel,
2000;Liu
tionsfrom
molecular-marker
isthatinferred
basedstudies
his- etal.,2001; Cronnetalt,2002; Cronnetal., 2003). These
torical
a commonsetofnatural
between
geneflowmaybe indicated
speciesthatshow studieshaveidentified
lineages
that
orreproductive
barriers
thatwouldappear arecongruent
strong
geographic
withgeographic
distributions
(Fryxell,
1992)
to prohibit
thesexualexchange
thatis inferred
tohavetaken andcytogenetic
withthe
'genome'designations
(abbreviated
place.Thesebarriers
includeextreme
geographic
isolation
as
letters
A-G andK; Endrizzietat, 1985),thelatter
ofwhich
well as intrinsic
barriers
to matingand geneticexchange are based on chromosome
size and pairingbehaviorin
& Soltis,1991;Rieseberg
& Wendel,1993;Arnold, interspecific
(Rieseberg
hybrids.
Ourcurrent
hypothesis
forphylogenetic
1997;Rieseberg,
1997).
ofthecottongenomegroupsissummarized
interrelationships
A caseinpointis Gossypium,
a moderately
sizedgenuswith inFig.1.
an aggregate
thatencompasses
globaldistribution
semiarid
to
Threeaspectsof the Gossypium
evolutionary
and genetic
aridregions
ofthetropics
andsubtropics.
Becausemostcot- history
arerelevant
tothetopicofcryptic
interspecific
hybridtonspeciesexistinrelatively
small,scattered
populations
that ization.First,theeightdiploidgenomegroupsexistas four
appearto be highly
inbred,
andbecausespeciestypically
are majorlineagesofspeciescorresponding
to threecontinents:
? NewPhytologist
www.newphytologist.org
(2003)161:133-142
New
Phytologist
review
Research
D
Americas
.......<
Africa
~@
Review 135
schwendimanii
?5lobatum
laxum
aridum
harknessii
armourianum
turneri
thurberi
trilobum
klotzschianum
davidsonii
Q-.J raimondii
4 gossypioideo nhirsutum
AD.
barbadense
darwinii
w0
.::; O arboreum
*..-*)%fherbaceum m ustelinum
F lOlongicalyx
anomalum
B capitis-viridis
triphyllum
E
stocksii
somalense
areysianum
incanum
vollesenii
nelsonli
G australe
bickii
of
framework
Fig.1 Phylogenetic
from
as inferred
genomegroups,
Gossypium
genes.Genome
nuclear
low-copy
multiple
robinsonii
sturtianum
cunninghamii
,r
Aut
AUStralia
puli7folium
areidentified
lineages
fordiploid
designations
/
ofcryptic
speciesthatshowevidence
bya solidcircle.
areidentified
introgression
as the
areidentified
cottons
Allotetraploid
of
affinity
andthephylogenetic
AD-genome,
areshown
ancestors
A-andD-genome
their
\
(A-CandK),andcotton
letter
bya single
circle.
with
a dotted
(C-, G-, K-genomes),
theAmericas(D-genome),Australia
(A-, B-, and F-genomes)and the Arabian
Africa/Arabia
in thegenus
The earliest
divergence
peninsula(E-genome).
theancestor
from
lineage
theNewWorldD-genome
separated
Old World
and
World
New
making
taxa,
World
Old
ofall
of
the high
Because
sister
groups.
diploidsphylogenetic
experimenlineages,
natural
these
between
divergence
genetic
betweena
crossescan onlybe accomplished
talinterspecific
cases,F1
all
in
species;
related
closely
of
limitednumber
etal.,
are
sterile
(Endrizzi
groups
genome
between
hybrids
and 12
datafromfourchloroplast
1985).Second,molecular
in
wereestablished
thattheselineages
genesindicates
nuclear
froma comdivergence
following
rapidsuccession
relatively
(Seelananetat, 1997;Cronnetat, 2002).The
monancestor
scenarioenvisionedis thattherewas a rapid
evolutionary
? NewPhytologist
(2003) 161: 133-142 www.newphytologist.org
marchantii
nobile
costulatum
K S2anapoides
chndonderriense
ellum
(
exlguum
piosum
rotundifolium
of thegenus,withtemporally
earlyin thehistory
radiation
theglobaldistribution
Finally,
events.
spaceddivergence
closely
(approx.
recent
tobe causedbyseveral
ofthegenusisbelieved
events
oceanicdispersal
yearsago)long-distance
5-10 million
examples
1992).Morerecent
1979;Wendel& Albert,
(Fryxell,
dispersaleventsincludethecolonization
of trans-oceanic
(tetraploid
suchas HawaiianArchipelago
ofinsularhabitats
G.darwinii,
Islands(tetraploid
theGalapagos
G. tomentosum),
andtheCapeVerdeIslands(diploid
diploidG. klotzschianum)
C. capitis-viridis).
shownin Fig.1 is
theframework
throughout
Distributed
casesofreticulaand unlikely
ofsixunexpected
a minimum
in
areimplicated
tionamongdiploidspeciesthatcollectively
orabout
of12species,
evolution
and/or
subsequent
theorigin
include:
ofthegenus.Thesecasesofincongruence
one-fourth
136
Review
review
Research
New
Phytologist
intotheparentage
2003) hasyieldedunprecedented
insight
and timingof polyploidcottonformation.
Low-copygene
sequencesin AD-genometetraploids
clearlysupportthe
ofallopolyploid
cottonandspecifically
genomic
origins
point
to A-genome
African
cottons(2 species)and thePeruvian
as theclosestliving
D-genomediploidspeciesG. raimondii
relatives
oftheancestral
genomedonors(Fig. 1). AdditioninheritedchloroplastDNA
ally,analysisof maternally
hamii(Seelanan etat, 1997; Seelananetat, 1999; Liu etat,
DNA (Small& Wendel,
2001);andthree
African
B-genome
diploidspecies,
G.anoma- (Wendel,1989) and mitochondrial
1999) identify
theAfrican
and G. troihyllum
parentas thematernal
lum,G. capitis-viridis
cytoplasm
(Cronnetal.,2002).
Theseputative
under- donor.
examples
ofcryptic
geneticexchange
clockarguments,
thesediploidprogeniscorea remarkable
feature
ofthegenus,namely,
for
Usingmolecular
potential
timeof6-7 millionyears
hybridization
between
lineagesthathaveno obviousoppor- torsshowan estimated
divergence
tunity
ofsexualcontact.It maybe thatoneormoreofthese ago (Cronnetat, 2002; Senchinaetat, 2003). Atthistime,
events
locahybridization
theformation
ofnewspecies, NorthAmericaand Africahad achievedtheirpresent
stimulated
D- andA-genome
between
as iscertainly
thecaseforallopolyploid
cottons.
Eachofthese tions,so theprimary
divergence
is discussed
inturnbelow.
examples
diploidgroupsclearly
involved
trans-oceanic
dispersal.
Using
in a comsimilar
logic,thesediploidgenomes
werereunited
monnucleusbypolyploidization
about1.5million
yearsago.
Intercontinental
dispersal,
allopolyploid
Long-distance
musthavefostered
coldispersal
thetransient
speciationandtheGossypium
tetraploids
ofanA-genome
onization
cottonin theAmericas,
leadingto
- Uplandcotton(G. hirsutum)
The cottons
ofcommerce
hybridization
withan indigenous
G. raimondii-like
and
diploid,
- represent
Pimacotton(G. barbadense)
extinction
oftheAfrican
twooffivenatural and thesubsequent
The
emigrant.
from nascent
allopolyploid
lineageradiated
intothree
branches
and
allotetraploid
speciesthatsharea singleorigin,
emerging
thechanceunionbetween
twodiploidspeciesthatevolvedin
fivemodern-day
species.
isolation
on separate
continents.
The worldwide
importance
ofthesespecieshasmotivated
scoresofresearchers
toattempt
Genomicchimerism
andthemultiply
hybrid
todecipher
themysteries
their
A synopsis
surrounding
origin.
ancestry
of
Gossypium
gossypioides
isshowninFig.1,andcanbefoundinWendel
ofthishistory
& Cronn(2003).
A striking
ofinterspecific
in Gossypium
example
sexualcontact
in Gossypium
Earlycytogenetic
surveys
notonlycytoplasmic
revealedthepre- involves
introgression
between
species,
senceoftwochromosome
levels,n = 13 and n = 26 (Wendel but apparentrecombination
betweendivergednuclear
& Cronn,2003). Critically,
itwasnotedthattheformation genomes(Wendeletalt,1995b; Cronnetat, 2003). The
of 13 bivalents
in triploid
between
wilddiploidand
hybrids
speciesin questionis G. gossypioides,
the sole memberof
cultivated
thehypothesis
thatthe subsectionSelera,which is restricted
tetraploid
species'support
to small, isolated
specieshaving26 pairsare allotetraploids',
and further populations
ina singleriver
inOaxaca,Mexico.
drainage
thattheancestral
suggested
diploiddonorsinvolved'wild
Untilrecently,
G.gossypioideswas
considered
unremarkable
American
species... andAsiaticspecies'(Webber,
1935).The
amongAmerican
as theinferred
diploidcottons,
relationships
allopolyploid
hypothesis
gainedsupportfromexperimental between
G.gossypioides
andotherD-genomespeciesbasedon
hybridizations
between
A-genome
(African)
and D-genome morphology,
cytogenetic
data,interfertility
relationships,
and
A x D F1 hybrids, allozymeanalysiswerecongruent
(American)
diploids.Newlysynthesized
(Wendeletat, 1995b).
whileinfertile,
couldbe colchicine-doubled
to produceself- Wendeletat (1995b), however,
showedthatthe nuclear
fertile
synthetic
AD-genometetraploids.
Significantly,
these ribosomalDNA sequencesfromG. gossypioides
are unlike
fertile
formed
amphiploids
withnatural
hybrids
AD-genome thoseofotherD-genomespecies.In fact,sequenceanalysis
In lessthan20 yr,thechromosomal
tetraploids.
composition showsthatG.gossypioides
isstrongly
as a member
resolved
of
of cottontetraploids
was identified
by morphometric
and
theAfrican
lineagethatincludes
A-,B-,and F-genome
cotcytogenetic
analysis.However,two significant
questions tons(Seelananetat, 1997;Cronnetat, 2003). Subsequent
remained
unanswered
by theseapproaches:
Whichdiploid to thisfinding,
G. gossypioides
was shownto containaddithe progenitors;
speciesbestrepresent
and whendid the tionalrepetitive
DNAs thataresharedwithAfrican
cotton
form?
tetraploids
speciesbutareunknown
amongAmerican
(D-genome)and
As mostnucleargeneshavebeenduplicated
in tetraploid Australian
(C- and G-genome)species(Zhao etat, 1998).
AD-genomecottons(Brubakeretal., 1999), sequence Complicating
thestoryfurther,
recent
phylogenetic
analyses
analysisof duplicateloci (Smalletat, 1998; Cronnetat,
basedon nuclear5S rDNA (Cronnetat, 1996) and eight
1999;Small& Wendel,2000a;Liu etat, 2001; Cronnetat,
nucleargenes(Small& Wendel,2000; Liu etat,
low-copy
fiveNewWorldAD-genomeallotetraploid
species(Wendel
etat, 1995a;Smalletat, 1998);twoNewWorldD-genome
diploid species, G. gossypioides
(Wendel etat, 1995b;
Seelananetat, 1997; Cronnetal., 2003) and G. aridur
(Wendel& Albert,1992,Alvarez& Wendel,unpublished);
bickii
twoAustralian
diploidspecies,G-genomeGossypium
(Wendeletal., 1991),andtheK-genome
speciesG. cunning-
? NewPhytologist
www.newphytologist.org
(2003) 161: 133-142
New
Phytologist
review
Research
Review 137
schwendimanhi
lobatum
laxum
:
I)
l
aridum
harknessii
armourianum
~turners
thurberi
cpDNAo? trilobum
tzchianum
~~~klo
davidsoniim
8
-'0raimondii
: gossypioldes
-nuclear
nucearcpDAO.***
l
in
andintrogression
Fig.2 Hybridization
twoseparate
Through
NewWorldcottons.
events,
hybridization
Gossypium
DNA
repetitive
nuclear
acquired
gossypioides
1), anda
source(progenitor
from
an African
similar
to
chloroplast
genomethatishighly
G. raimondii
2). In
modern-day
(progenitor
Colima,Mexico
from
G. aridum
addition,
genomethatis
possesesa chloroplast
from
allmembers
ofSubsection
divergent
showsthat
analysis
Phylogenetic
Erioxylum.
to
genomehasa highaffinity
thischloroplast
andG. klotzschianum,
G. davidsonii
a hybridization
eventbetween
implicating
species.
thesedivergent
L~2
repetitive
DNA
A
:1
D
E
CIGIK
2001; Cronnetat, 2003) reveals
thatG.gossypioides
occupies Subsequent
backcrossing
ofthishybrid
totheG.gossypioidesthebasalpositionwithintheD-genomeclade.This finding likeancestor
restored
thesingle-copy
component
oftheDcontrasts
withexpectations
from
morphology
(Fryxell,
1971), nucleargenome,butfailedto purgeall 'African'
repetitive
interspecific
hybridization
studies(Brown& Menzel,1952;
elements.
Morerecently,
hybridization
witha Mexicanspecies
Menzel& Brown,1954),andevidence
fromthechloroplast similarto modern-day
G. raimondii
(presently
restricted
to
genome(Wendel& Albert,1992;CronnetaL,2003),allof
Peru)resulted
incpDNA introgression,
andperhaps
a second
whichidentify
a closetiebetweenG. gossypioides
and G. rai- roundofcryptic
nuclearintrogression
(Cronnetal.,2003).
thelatter
ofwhichoccupiesa terminal
mondii,
phylogenetic Regardless
ofthedetailsofthismysterious
G.gosancestry,
position
withintheD-genomeassemblage
(Small& Wendel, sypioides
the potentialforgenomic'chimerism'
highlights
2000; Cronnetat, 2003).
within
a diploidspeciesforwhichno evidence
ofreticulation
Thesedataimplicate
a complexhistory
forG.gossypioides,wasdetected
beforemolecular
investigation.
Indeed,present
one thatincludestwo temporally
separatedintrogression geographic
rangedistributions
and geneticisolationmechaeventsinvolving
genetically
divergent
cottonsthatare pre- nismswouldsuggest
thatthehybridization
eventsimplicated
sentlyrestricted
to different
hemispheres
(Fig.2). Basedon
are implausibleif not impossible.Yet the evidencefor
repetitive
nuclearDNA, itappearsthatG.gossypioides
experi- genomiccontactis compelling
and alternative
explanations
encednuclearintrogression
froman African
speciesshortly havenotemerged.
Thisexamplealsoillustrates
thephylogeafter
fromtheAmerican
divergence
assemblage.
Thishybrid- neticcomplexity
thatcanresult
from
multiple
historical
reticuizationeventeither
occurred
at thediploidlevelorat thetri- lationevents,
andthusserves
as a sobering
cautionary
talefor
ploidlevel,possibly
as a consequence
ofhybridization
with inferences
of history
basedexclusively
on onlyone or two
theNewWorldallopolyploid
lineage(Wendeletal., 1995b). sources
ofmolecular
evidence.
?DNewPhytologist
(2003)161:133-142 www.newphytologist.org
138
Review
New
Phytologist
Research
review
A
F
B
E
cpDNA,...-** ~@
* .....
cpDNA
K
nelsonii
australe
bickii
robinsonfi
sturtianum
cunninghamii
populifolium
marchantii
in
andintrogression
Fig.3 Hybridization
nobile
Australian
cottons.
TheG-genome
species
costulatum
/
._
bickii(from
SectionHibiscoidea)
Gossypium
anapoides
and K-genomespeciesG. cunninghamii
(SectionGrandicalyx)
eachpossessa
londonderriense
chloroplast
genomethatisuncharacteristic
pulchellum of
theirrespective
taxonomic
Sections.
enthyle
showsthesechloroplast
a\_J " 'gw
Phylogenetic
analysis
tomodern-day
similar
tobe highly
sequences
exiguum
G.sturtianum,
pilosum
implicating
independent
chloroplast
transfer
eventsbetweenthese
rotundifolium
lineages.
divergent
sturtianumiG.
robinsonii.
This
is explainedby
discrepancy
Othercases ofcryptic
hybridization
between
invoking
a bi-phyletic
ancestry
forG. bickii,
a G.
whereby
allopatric
Gossypiumspecies
sturtianum-like
speciesservedas thematernal
parentin an
Inaddition
toG.gossypioides,
three
additional
diploid
species ancienthybridization
witha paternal
donorfromthelineage
inGossypium
areimplicated
tohaveexperienced
cytoplasmicleadingto G.australeand
G. nelsonii,
whichisshowninFig.3.
transfer
byvirtue
of incongruent
cpDNA/nuclear
data To date,G. sturtianum
and G. robinsonii
alleleshaveyettobe
(Fig.3).Thefirst
wasdiscovered
a phylogenetic
during
study detectedin G. bickii,suggesting
thatthenucleargenomic
ofAustralian
where
species,
molecular
markers
from
the contribution
ofthematernal
parent
waseliminated
fromthe
plastid
andnuclear
genomes
anunusual
revealed
evolutionary
hybrid
oritsdescendent
lineage.
history
forG. bickii
(Wendel
etal.,1991;Seelanan
etal.,
A similar
exampleof'cytoplasmic
capture'
hasbeenimpli1999;Liu etal.,2001).Thisspecies
is one of three catedfortheAustralian
K-genome
cottonG. cunninghamii.
morphologically
similar
G-genome
cottons,
alongwithG. Thisspecieshasanunusualmorphology
andisgeographically
australe
andG. nelsonii
(Fryxell,
insection disjunctfromall otherK-genomespecies,in thatit is
1971)included
Hibiscoidea.
By contrast
to expectations
basedon this restricted
to the CobourgPeninsulaof Australiaapprox.
taxonomy,
thechloroplast
genome
ofG.bickii
wasshown
to 500 kmdistant
from
theKimberley
region
wheretheremainbenearly
identical
totheplastid
genome
ofG.sturtianum
and ingspeciesarefound.Analogousto G. bickii,
thechloroplast
G. robinsonii,
a pairofmorphologically
distant
C-genome genomeofG. cunninghamii
appearstohavebeendonatedby
from
species
section
Sturtia.
Bycontrast,
nuclear
markersa G. sturtianum-like
ancestor(Fig.3), althoughin thiscase
reveal
theexpected
relationship,
that
is,that
G.bickii
shares
a thehybridization
eventappearsto havebeenmoreancient
more
recent
common
ancestor
with
itsclosemorphological
(Wendel& Albert,1992; Seelananetal., 1999; Liu etal.,
allies(G. australe
andG. nelsonii)
thanit doeswithG. 2001).AswithG. bickii,
nuclear
ribosomal
DNA (Wendel&
www.newphytologist.org? NewPhytologist(2003)
161: 133-142
New
Phytologist
review
Research
Review 139
A
F
B
_ anomalum
capitis-viridis
triphyllum
E
in
andintrogression
Fig.4 Hybridization
African
cottons.
markers
identify
Nuclear
ofa
theB-genome
lineageas a member
DNA?)
(nuclear
cpDNA
D
p
Africanlade thatincludes
monophyletic
A-andF-genome
species.Nevertheless,
ofB-genome
phylogenetic
analysis
DNAshowsthislineageto be the
chloroplast
C- andG-genome
sister
groupofAustralian
a chloroplast
transfer
cottons,
implicating
ofthese
eventbetweentheprogenitor
Australian
cottons
andtheprogenitor
ofBInaddition
to molecular
genomecottons.
isunusual
B-genome
markers,
G. triphyllum
ofmorphological
inthatitdisplays
a number
species.
to G-genome
restricted
features
*
Anelson)I
.
3
bickll
se
bickii
C
K
Albert,
1992;Seelananetal., 1999)andthelowcopynuclear examples,
theextantspeciesthatbestrepresent
theputative
geneFAD2-1 (Liu etal., 2001) showthatG. cunninghamii cytoplasmic
donor(G. davidsonii
and G. klotzschianum)
show
sharesa morerecentcommonancestorwithitsK-genome geographic
ranges
(BajaCalifornia
andtheGalapagosIslands,
relatives
thanitdoeswithG.sturtianum
(Seelananetal, 1999;
respectively)
thataredistant
from
modern-day
G. aridum
and
Liu etal, 2001).
are reproductively
isolatedfromG. aridumby intrinsic
A finalexampleofcryptic
introgression
at thespecieslevel geneticbarriers.
is seenin G. aridum,
one offourspeciesofMexicancottons
thatcomprise
subsection
ThesespeciesaredistincFrioxylon.
B-genome,Africancottons- an additional
tivesmalltrees,and theirsharedcommonancestry
is supancient
event?
introgression
portedbynearly
all studiesto date(Fryxell,
1971; DeJoode,
1992;Wendel& Albert,1992;Wendeletal., 1995b;Cronn Threesub-Saharan
cottonspeciescomprisethe B-genome
etal., 1996; Small& Wendel,2000). The soleexception
to
diploid group,includingG. anomalum(widespreadin
thisunanimity
isthatG. aridum
populations
fromtheMexi- northern
Africa),its sisterspeciesG. capitis-viridis
(Cape
can stateofColimahavea chloroplast
genomethatis strik- Verde Islands),and the morphologically
distinctiveG.
inglydivergent
fromotherpopulations
of G. aridumandthe triphyllum
(Angola,Botswana,
and Namibia).Thesespecies
otherthreespeciesin subsection
Erioxylon
(DeJoode,1992;
form a geneticallycohesive group within a larger,
Wendel& Albert,
1992).Curiously,
thischloroplast
genome monophyletic
lineageof Africancottonsthatincludesall
showshighsequencesimilarity
to thechloroplast
genomeof speciesin theA-, B- and F-genomegroups(Fig.4). The
G. davidsonii
and G. klotzschianum,
twospeciesfrom
a differ- associationbetweentheB-, A- and F-genomegroupswas
enttaxonomic
section(Integrifolia)
thatarestrongly
differen- long suspected,since theysharea commongeographic
tiatedat themorphological
(Fryxell,
1971) andgeneticlevel distribution,
distinctively
intermediate
genomesizes(3.3(Endrizzietal., 1985; Cronnetal., 2003). The apparently 4.2 pg/2C),and similarchromosome
pairingbehaviorin
'alien'cytoplasm
in Colima G. aridumis inferred
to have interspecific
crosses(Endrizzietat, 1985). On thebasisof
arisenby introgressive
hybridization
witha memberof the these characteristics,
Fryxell(1971, 1992) included G.
Integrifolia
subsection,
asshowninFig.2. Asinthepreceding anomalum
and G. capitis-viridis
as members
ofthesubgenus
( New Phytologist
(2003) 161:133-142
www.newphytologist.org