Plant speciation in continental island floras as exemplified by Nigella in the Aegean Archipelago

14 Pages·2008·0.63 MB·English

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Phil.Trans.R.Soc.B(2008)363,3083–3096
doi:10.1098/rstb.2008.0063
Publishedonline25June2008
Plant speciation in continental island
floras as exemplified by Nigella
in the Aegean Archipelago
Hans Peter Comes1,*, Andreas Tribsch1 and Christiane Bittkau2
1Fachbereich fu¨rOrganismische Biologie, Paris-Lodron-Universita¨tSalzburg,
5020Salzburg,Austria
2Institut fu¨rSpezielle Botanik undBotanischer Garten,
Johannes Gutenberg-Universita¨tMainz,55099 Mainz, Germany
Continental shelf island systems, createdby rising sea levels, provideapremier setting for studying
the effects of geographical isolation on non-adaptive radiation and allopatric speciation brought
about by genetic drift. The Aegean Archipelago forms a highly fragmented complex of mostly
continental shelf islands that have become disconnected from each other and the mainland in
relatively recent geological times (ca !5.2Ma). These ecologically fairly homogenous islands thus
provide a suitable biogeographic context for assessing the relative influences of past range
fragmentation, colonization, gene flow and drift on taxon diversification. Indeed, recent molecular
biogeographic studies on the Aegean Nigella arvensis complex, combining phylogenetic,
phylogeographicandpopulationlevelapproaches,exemplifytheimportanceofallopatryandgenetic
drift coupled with restricted gene flow in driving plant speciation in this continental archipelago at
differenttemporalandspatialscales.Whiletherecent(LatePleistocene)radiationofAegeanNigella,
as well as possible instances of incipient speciation (in the Cyclades), is shown to be strongly
conditionedby(palaeo)geographicfactors(includingchangesinsealevel),shiftsinbreedingsystem
(selfing) and associated isolating mechanisms have also contributed to this radiation. By contrast,
founder event speciation has probably played only a minor role, perhaps reflecting a migratory
situation typical for continental archipelagos characterized by niche pre-emption because of a long
establishedresidentflora.Overall,surveysofneutralmolecularmarkersinAegeanNigellahavesofar
revealedpopulationgeneticprocessesthatconformremarkablywelltopredictionsraisedbygenetic
drifttheory.Thechallengeisnowtogainmoredirectinsightsintotherelativeimportanceoftherole
of genetic drift, as opposed to natural selection, in the phenotypic and reproductive divergence
among these Aegean plant species.
Keywords:Aegean palaeogeography;allopatric speciation; continental shelf islands; genetic drift;
Nigella;non-adaptive radiation
1.INTRODUCTION see Linder 2008). In most cases, such radiations have
Thetermspeciesradiation,i.e.thedivergentevolution been attributed to ecological opportunities afforded
of a relatively large, monophyletic group of species by the emergence of new habitats and the absence
within a relatively short time (Stanley 1979; Schluter of competition on recently formed oceanic islands
2000),ismostfrequentlyusedincombinationwiththe and continental mountain ranges, rather than to the
epithet ‘adaptive’ (Givnish 1997), which in turn evolution of key morphological or physiological inno-
implies ecological specialization and the probable vations (but see Klaket al.2003;Kayet al.2005).
co-occurrence of closely related species (MacArthur By contrast, only a very few studies have explicitly
1972; Schluter 2000; Savolainen & Forest 2005). In addressed the question of whether species prolifera-
recent years, molecular phylogenetic data have pro- tion might occur by ‘non-adaptive radiation’ (sensu
vided a number of spectacular examples of explosive Cain1944;Givnish 1997;Savolainen &Forest2005),
adaptive species radiations for plants in the recent i.e. without appreciable ecological divergence and
evolutionarypast(LateTertiary/Quaternary),oneither evolution of corresponding adaptations, and simply
as a consequence of geographical isolation and allopa-
oceanic islands (Baldwin & Sanderson 1998; Bo¨hle
tric divergence among sibling species maintaining
et al. 1996; see also Whittaker & Ferna´ndez-Palacios
similarecologicalnichesoverevolutionarytimescales.
2007) or continents (Richardson et al. 2001; Klak
Such an allopatric model of non-adaptive species
etal.2003;Kayetal.2005;Hughes&Eastwood2006;
radiationessentiallyimpliesthatmutationandrandom
genetic drift, rather than habitat-mediated selection,
*Authorforcorrespondence([email protected]). will be the primary factors causing divergence of
populations occupying ecologically similar habitats.
Onecontributionof12toaThemeIssue‘Speciationinplantsand
animals:patternandprocess’. The best-known examples include species-rich taxa of
3083 Thisjournalisq2008TheRoyalSociety
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3084 H. P.Comeset al. AegeanNigella speciation
N. a. arvensis
N. a. glauca
N. a. aristata
N. d. barbro
N. icarica
N. d. jenny
N. d. degenii
N. a. brevifolia
N. d. minor
N. stricta N. a. brevifolia
N. carpatha
km
N. a. brevifolia N. doerfleri
0 50 100
Figure1.Approximatedistributionrangesofthesixspecies(12taxa)oftheAegeanNigellaarvensiscomplex(afterStrid2002;
see also table 1). Solid versus dashed lines delineate outcrossing versus selfing taxa. Note that the range of N. arvensis ssp.
brevifoliaonCretecomprisesonlyfourknownpopulations.N.a.,N.arvensis;N.d.,N.degenii.
land snails on either Crete (Albinaria: Gittenberger Ferna´ndez-Palacios 2007). However, based on their
1991; Giokas 2000) or the Madeiran island of Porto thorough reassessment of the speciation literature,
Santo (Helicidae: Cameron et al. 1996), as well as Coyne& Orr(2004,pp.383–410)recently concluded
particular plant lineages in the Aegean Archipelago thatfirmempiricalevidenceforaroleofgeneticdriftin
(e.g. Snogerup 1967; Strid 1970; Stork 1972; see §2). speciation is rare, and they also raised the same
In addition, Savolainen & Forest (2005) claimed objection about drift-induced peripatric or founder-
that the term non-adaptive radiation might also be effect speciation. Also, mathematical models indicate
an appropriate way of describing the diversification that conditions for speciation via drift are fairly
of the temperate legume genus Astragalus (see also restrictive (Barton 1996; Coyne et al. 1997; Turelli
Sanderson & Wojciechowski 1996; Sanderson 1998).
et al. 2001; Coyne & Orr 2004). For example, while
Similarly, Whittaker & Ferna´ndez-Palacios (2007)
showing that geographical isolation can lead to
hypothesized that a non-adaptive component might
complete reproductive isolation (Nei et al. 1983),
beresponsiblefortheradiationofseveralMacaronesian
such models have also revealed that even a small
plantgenera(i.e.Cheirolophus,Helianthemum,Limonium)
amount of gene flow can retard differentiation by drift
that exploit similar habitats in different islands.
(Coyne & Orr 2004, p. 87). Moreover, genetic drift is
Althoughasystematicsurveyoftheirprevalencewould
generally thought to cause speciation and quantitative
be valuable, it is perhaps no coincidence that most
phenotypic evolution more slowly than does either
cases proposed for non-adaptive radiation are from
directionalselectionaloneorincombinationwithdrift
island systems. In such geographical settings, random
(Coyne et al. 1997). On the other hand, there is good
genetic drift (whether in established populations or
evidence for a role of genetic drift in chromosomal
during founder events) has long been implicated as
speciation, particularly in plants (Rieseberg 2001).
contributingtospeciationviz.reproductiveisolationand
Again, especially within plants, a probable important
phenotypic evolution (e.g. Mayr 1954; Carson 1975;
mechanism favouring speciation by drift is selfing,
Templeton1980;seealsoGrant1998).
which has recently been invoked in a study of arctic
Although patterns of molecular variation in island
Draba species as providing an efficient non-adaptive
populations often do correspond to what would be
expected if the loci were affected by genetic drift (e.g. means for the accumulation of intraspecific hybrid
Wendel & Percival 1990; Barrett 1996; Berry 1996; incompatibilities (Grundt et al. 2006). Another well-
Stuessy et al. 2006), the contribution of genetic drift known, but fairly unusual, example for speciation by
to island speciation remains the subject of keen drift involves shell coil reversals in land snails
debate (e.g. Barton 1996; Grant 1998; Whittaker & (Gittenberger 1988; Ueshima &Asami 2003).
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AegeanNigella speciation H. P.Comeset al. 3085
Table1.Geographicaldistribution,habitatpreference,floweringperiodandbreedingsystemofthetaxaoftheNigellaarvensis
complex (after Strid1970and modified accordingto Bittkau& Comesinpress).Note that mosttaxaoccur atlowaltitudes
(approx.0–500ma.s.l.)exceptforNigellaarvensisssp.glauca(0–1000ma.s.l.)andNigellaicarica(500–1000ma.s.l.).
geographical flowering breeding
Nigellataxon distribution habitat period system
N.arvensisL.
ssp.arvensis NGreece/EuropeandNAfrica cultivated/abandonedfields VI–IX outcrosser
ssp.aristata(Sibth. SandCGreekmainland,Euboea phrygana,abandonedfields,roadsides mid-V–VII outcrosser
andSm.)Nym.
ssp.glauca(Boiss.) EAegeanislands,WTurkey, phrygana,abandonedfields,olive VI–VIII outcrosser
Terracc. Thrakia groves
ssp.brevifoliaStrid Elafonisos(southofPeloponnisos) phrygana,abandonedfields,roadsides VI–VIII outcrosser
WCretea,Rhodes
N.carpathaStrid SKarpathos,Kasos phrygana mid-V–mid-VII outcrosser
N.degeniiVierh.
ssp.degenii CandSCycladesb phrygana,cultivatedfields,seashores VI–VII outcrosser
ssp.barbroStrid NWCyclades(Andros,Tinos, phrygana,roadsides,seashores mid-V–mid-VII outcrosser
Mikonos)
ssp.jennyStrid NWCyclades(Siros) phrygana,abandonedfields end-V–mid-VI outcrosser
ssp.minorStrid SCyclades(Pakhia,southof phrygana end-V–VI outcrosser
Anafi)
N.icaricaStrid Ikaria phrygana VI–VII outcrosser
N.doerfleriVierh. Andikithira,Cyclades,Crete phrygana end-IV–mid-V selfer
N.strictaStrid Kithira,SWCrete stablesanddunes mid-IV–mid-V selfer
aKnownfromonlyfourlocationsonCrete(Strid1970;Z.Kypriotakis2002,personalcommunication).
bKnownfromthefollowingislands:Amorgos,Andiparos,Folegandros,Kimolos,Milos,Naxos,Paros,Santorin,Sifnos,Sikinos.
There can be no doubt that natural (and sexual) islands(Sumatra,Java,Borneo),andtheNorthPacific
selection plays a much larger role in speciation and Vancouver and Queen Charlotte islands). Such island
phenotypicdiversificationthandoesdrift(e.g.Macnair& systemshavemanyoftheadvantagesofoceanicislands
Gardner 1998; Rieseberg et al. 2002; Coyne & Orr (e.g. Hawaii, Gala´pagos, Canaries) in that they allow
2004;Waser&Campbell2004;Johnson2006;Noor& insights into colonization and restricted gene flow. As
Feder2006;seeLexer&Widmer2008).Nonetheless, an important difference, however, continental islands
it would seem to be premature to close the book on alsoprovideapremiersettingforstudyingtheeffectsof
speciation by drift, no less than dismissing its role in past range fragmentation via geologically dated sea
phenotypic evolution at all. Rather, considering both barriers, and thus for testing genetic drift-models of
theoryandempiricalevidence,apotentialroleofnon- allopatric speciation and non-adaptive radiation
adaptive radiation by drift will still apply to all species (Wright 1940;Mayr1954; Schluter 2000).
occurring in effectively isolated (allopatric) popu- In fact, the most suggestive evidence for non-
lations, especially if these are permanently or tempor- adaptiveradiationcomesfromplantgroupsinhabiting
arily small (Wright 1948; Slatkin 1985). Yet, despite the ecologically fairly homogenous continental island
allopatric speciation being widely considered as the system of the Aegean Archipelago (Runemark 1969;
most common geographical mode (Barraclough & Strid 1970; Barrett 1996; Levin 2000). This claim,
Vogler 2000; Turelli et al. 2001; Coyne & Orr 2004), specifically, relates to the biosystematic work of Strid
and notwithstanding an expanding literature on the
(1970) conducted on the so-called Nigella arvensis
joint roles of allopatry and ecology in speciation
complex (Ranunculaceae, tribe Nigelleae), which
(Schluter 2000; Ogden & Thorpe 2002; Wiens 2004;
contains six species (12taxa) that are mostly allo-/or
Kozak & Wiens 2006; Thorpe et al. 2008), the
parapatrically distributed on numerous islands and
relationship between geographical isolation, drift,
adjacent mainland areas of Greece and western
phenotypic differentiation and reproductive isolation
Anatolia (figure 1, table 1). Based on crossing experi-
remains poorly understood in ‘non-ecological specia-
ments, aswellas morphological and palaeogeographic
tion’ (sensu Schluter 2000).
evidence, Strid (1970) argued that differentiation in
the N. arvensis complex has been determined princi-
2.THE AEGEAN ARCHIPELAGO ASA pally by two factors: (i) range fragmentation triggered
LABORATORY OFALLOPATRICSPECIATION by Plio-/Pleistocene changes in sea level; and
AND NON-ADAPTIVE RADIATION (ii) subsequent evolution of the fragmented ancestral
Perhaps the most suitable natural laboratories for stockviageneticdriftviz.non-adaptiveradiation.Strid
studying the effects of geographical isolation on (1970) further hypothesized that genetic drift in the
allopatric speciation are ‘continental shelf islands’ complexislargelybroughtaboutbydrasticpopulation
(sensu Whittaker & Ferna´ndez-Palacios 2007) that bottlenecks in established populations because of
have become disconnected from each other and/or (seasonal) fluctuations in population size rather than
the mainland in relatively recent geological times (e.g. by repeated interisland (or mainland-island) founding
mostAegeanislands,theSouth-EastAsianSundashelf colonizations. His contemporaries working on other
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3086 H. P.Comeset al. AegeanNigella speciation
endemic components of the Aegean flora favoured high degree of human-mediated secondary sympatry
similar evolutionary scenarios (e.g. Snogerup 1967; of plant populations, and thus may create an obstacle
Stork1972;Bentzer1973;VonBothmer1974,1987). to the interpretation of extant biogeographic and
Here, we will synthesize data from our recent and molecular patterns in the Aegean region. In the
ongoing molecular biogeographic studies of the N. arvensis complex, however, there is only limited
N. arvensis complex using phylogenetic, phylo- sympatry (except for a pair of species in the Cyclades;
geographic and population level approaches in order see §4), as would be predicted under a scenario of
todissecttheevolutionaryhistoryofthisplantgroupat non-adaptiveradiation.
increasingly smaller temporal and spatial scales. We
will first introduce the Aegean region, its palaeo- (b)Aegean palaeogeography
geographic history and our study group, and then Paleogeographic/climatic changes affecting the entire
giveaconciseoverviewofthemainresults,withafocus MediterraneanbasinduringtheLateTertiary/Quatern-
on the times and orders of evolutionary divergence aryhavelikelyexertedamajorinfluenceonthepatterns
within the complex, and the population genetic ofgeographicalisolationandallopatricspeciationinthe
processes underlying its supposedly non-adaptive N. arvensis complex. Of particular relevance is the fact
radiation. In essence, our data indicate that allopatry thatseveral palaeogeographicevents providemaximum
(often but not exclusively vicariant) and genetic drift timesofisolationbetweentheAegeanislandsfromeach
(coupled with restricted gene exchange) are the other andthemainland. Inthisrespect, the ‘Messinian
dominant evolutionary processes driving population salinitycrisis’(ca6.0–5.3Ma;Duggenetal.2003)clearly
differentiation and speciation in Aegean Nigella. sets an upper time boundary for the last, large-scale
Because of lack of comparable data, however, we are reconnection of the entire region. During this time
presently far from being able to evaluate whether this period,theMediterraneancompletelydriedupasaresult
scenario also holds for other plant radiations in the oftheclosingoftheStraitofGibraltar,andtheAegean
Aegean Archipelago or similarly complex continental islands then became mountains in a steppe or desert
island systems. Moreover, as a critical limitation, our (Blondel & Aronson 1999). At some 5.2G0.1Ma, the
surveys of neutral molecular polymorphisms alone Strait of Gibraltar reopened and the basin was refilled
providelittledirect insight intothepotentialevolution- fromtheAtlanticOceanwithin1000years(Duggenetal.
ary processes (drift versus selection) and genetic 2003).Asaresult,oneofthefirstAegeanseabarriersto
changes causing phenotypic differentiation and repro- become permanently established was the East Aegean
ductive isolation in our study group. We conclude, Sea, separating the modern Cyclades from the east
therefore, with some current and possible future Aegeanislands(ca4.5Ma;Chatzimanolisetal.2003).
approachesfor tacklingthese more difficult issues. The sequence of Plio-/Pleistocene island formation
is particularly well documented for ‘Hellenic Arc’
islands. As another consequence of post-Messinian
3.THE STUDY AREA AND ITS flooding, Crete became isolated, and it has remained
PALAEOGEOGRAPHIC HISTORY isolated since; Kithira, however, was completely
(a) The Aegean Archipelago submerged and did not re-emerge until the late
The Aegean Archipelago (figure 1) is located between Pliocene (ca 3.0Ma; Meulenkamp et al. 1972). At
the Greek peninsula in the west and the Turkish coast about the same time, Karpathos became permanently
of Asia Minor in the east.Approximately 611kmlong disconnected from Rhodes-Anatolia (Daams & Van
and 299km wide, the total area of the Aegean Sea is der Weerd 1980), while the permanent separation of
some 214000km2, whereby the total area of the RhodesfromAnatoliaoccurredatthePlio-/Pleistocene
multitude of Aegean islands and islets (O100) is boundary(ca 2.4Ma; Kuss1975).
approximately 9012km2 (Strid 1997, 2002). Geo- For much of the remainder of the archipelago, the
graphically,theseislands can be roughly arranged into Quaternarysea-levelrecordcanbeusedtoapproximate
fourgroups:(i)EuboeaandtheSporades,agrouplying timesofislandseparation.Duringtheglacialperiodsof
off mainland Greece; (ii) the east Aegean islands, theRiss(250–125ka)andWu¨rm(75–10ka),sealevels
includingIkariaandSamos,lyingofftheTurkishcoast; were,respectively,200and120mlowerthanatpresent
(iii) the Cyclades, including 16 major islands such as (Sfenthourakis 1996; Perissoratis & Conispoliatis
Andros, Tinos, Mikonos, Siros, Paros, Naxos and the 2003). Thus, because of shallow sea barriers, Euboea
volcanic island of Santorin/Thera (from north to andseveraleastAegeanislands(e.g.Samos) havebeen
south); and (iv) the southern Aegean (‘Hellenic Arc’) separated from the nearby mainland only after the last
islands, including Kithira, Crete, Karpathos, Kasos glacial maximum (LGM; 23–18ka). The seafloor
and Rhodes, which mark the southern boundary of between Samos and Ikaria, however, is much deeper
the archipelago. (albeit less than 200m), so these neighbouring islands
Ecologically, the commonest habitat type in these were already separated by the sea transgression
islandsisatypicaldryMediterraneanmaquis-phrygana following the Riss glacial (Beerli et al. 1996).
community of evergreen, mostly degraded (under) AsregardstheCyclades, most oftheseislands once
shrub vegetation (Blondel & Aronson 1999), which is formed a landmass that remained connected to main-
also one of the most important habitats for the land Greece/Euboea until the end of the Pliocene
N. arvensis complex. Concomitantly, this vegetation (ca 2Ma; Fattorini 2002; Chatzimanolis et al. 2003).
type reflects the influence of humans on all aspects of During the glacial/interglacial periods of the Pleisto-
the environment that dates back to more than 5000 cene, most central islands were alternately joined and
years BP (Broodbank 2000). This may have led to a disentangled, with the most recent fragmentation
Phil.Trans.R.Soc.B(2008)
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AegeanNigella speciation H. P.Comeset al. 3087
dating back to late-glacial/Early Holocene times Inaccordancewithoneofthemajorcriteriafornon-
(Lambeck 1996). Notably, several Cycladic islands adaptive radiation, the habitats occupied by most taxa
further south (e.g. Milos, Santorin/Thera, Anafi) have of the N. arvensis complex vary little among islands or
been formed by volcanic activity that started in the the mainland (table 1). At least from a macro-habitat
Pliocene, and most of them were temporarily con- perspective, these taxa are ecologically unspecialized
nected to nearby islands during some period of their withpopulationsoccurringinawidevarietyofmoreor
existence (Sfenthourakis 1996). As will be seen in §7, less disturbed habitats (0–1000m a.s.l.) such as stony
the Cyclades’ intricate configuration and post-glacial seashores, phrygana communities, abandoned/culti-
palaeogeography offers an outstanding context in vatedfieldsorroadsides.Incontrasttotheoutcrossers,
which to explore the times and orders of recent however, the two selfers tend to occupy or tolerate
population splitting in a Nigella species endemic to morearidhabitats(Strid1969,1970),includingstable
these islands. sand dunes (N. stricta) or phrygana sites on small, dry
and isolated islands (N.doerfleri).
4.THE MODEL SYSTEM: THE NIGELLAARVENSIS
COMPLEX 5.SPECIES-LEVEL PHYLOGENETICSAND
(a) Breeding system and experimental PHYLOGEOGRAPHY
crossing barriers (a)Phylogenetics
Nigella is a genus of approximately 23 annual, diploid A recent molecular-phylogenetic study (Bittkau &
(2nZ12) and self-compatible species of mainly Med- Comesinpress),withacompletespeciesrepresentation
iterranean/Southwest Asian distribution (Strid 2002). ofNigellas.lat.(ZNigellaanditssistergenusGaridella)
The six species (12taxa) of the N. arvensis complex and based on internal transcribed spacer (ITS)
(figure 1, table 1) are mainly distinguished by flower sequencesofnuclearribosomalDNA,revealedthatthe
andfruitcharactersand,toalesserextent,byvegetative N.arvensiscomplextrulyqualifiesasa‘radiation’.The
characters,alwaysincombinationwiththeirgeographi- clock-calibrated ITS phylogeny generated showed
caldistribution(Strid1970).Fourspecies(N.arvensis, that all the species of the complex began diverging
Nigella carpatha, Nigella degenii, Nigella icarica) are rapidly from a single ancestor in the Late Pleistocene,
summer-flowering and predominantly outbreeding, between ca 0.78 (G0.39) and 0.16 (G0.08)Ma,
whereas self-pollination is the normal condition in the whereas the origin of this ancestor could only roughly
spring-flowering, smaller-sized Nigella doerfleri and beapproximatedtobetween6.2and1.3Ma(Messinian
Nigella stricta, because their styles regularly twist to mid-Pleistocene). In addition, both log lineages-
around the dehiscing anthers (Strid 1969). Attempts through-time(LTT)plots(Harveyetal.1994;Neeetal.
to produce fertile hybrids between N. doerfleri and 1994) and likelihood survival analyses (Paradis 1998)
N. stricta, or between the selfers and outcrossers, have indicated that the proliferation of Nigella species in the
been unsuccessful, whereas species of the latter group Aegean region caused a significant departure from a
are interfertile, with pollen-fertility values in hybrids stochastic, speciation–extinction process of diversifica-
ranging between 30 and100% (Strid 1970). tionduringtheevolutionofNigellas.lat.Otherwise,the
genuswouldhavefolloweda‘constant-ratesbirth–death’
(b)Geographicaldistributionand habitat (CR-BD)model(Harveyetal.1994;Barraclough&Nee
The10taxaoftheoutcrossingspeciesexhibitastriking 2001), a scenario under which speciation rate and
allo- or parapatric pattern of geographical distribution extinctionrateareassumedtobeconstantacrosslineages
(figure 1, table 1). The four outcrossing subspecies of withinaphylogenyandovertime(thenullhypothesis).
N.arvensisaredistributedintheformofaringaround Finally,wecouldshowthattheobservedupturncurvein
the Cyclades: ssp. aristata occurs in southern Greece, theLTT-plottowardsthepresent,mainlyassociatedwith
ssp.arvensisinnorthernGreece,ssp.glaucaintheeast theAegeanN.arvensiscomplex,wasmuchmorerecent
Aegean islands and Anatolia, and ssp. brevifolia is thanwouldhavebeenexpectedundertheCR-BDmodel
disjunctlydistributedonthe‘HellenicArc’(Elafonisos, (Bittkau&Comesinpress).Thisfindingindicatesthat
Crete, Rhodes). The three remaining outcrossing the recent radiation of the Aegean group truly reflects
species are island endemics: N. carpatha is found on an increase in the rate of speciation and not decreased
Karpathos (and nearby Kasos), N. icarica on Ikaria, extinction(Barraclough&Nee2001).Thus,themajor
and N. degenii is widespread throughout the Cyclades, hypothesis emerging from this molecular-phylogenetic
where four allopatric subspecies are recognized which study is that the accelerated rate of speciation in
are endemic to island groups (spp. barbro, degenii) or the Aegean N. arvensis complex is possibly related
single islands (spp. jenny, minor). Like the outcrossing to increased opportunities for allopatric speciation
taxa,theselfingspeciesarealsonotsympatricwithone afforded by the (palaeo)geographic complexity of the
another: N. stricta is restricted to Kithira and south- archipelago, combined with Late Pleistocene changes
western Crete, whereas N. doerfleri is more wide- inclimateandsealevel(Bittkau&Comesinpress).
spread (Andikithira, central/eastern Crete, Cyclades,
numerous small islets). The broad range overlap (b) Phylogeography
between N. doerfleri and N. degenii in the Cyclades is For plant groups inhabiting continental island
exceptional for the entire complex (figure 1). It thus systems, the smaller effective population size of their
appears that only species of the complex that differ in chloroplast (cp)DNA, compared with the nuclear
breeding system (and associated traits) are able to live genome(Birkyetal.1989),shouldbeparticularlyuseful
insympatryonthesameislands. for detecting signatures of past range fragmentation
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3088 H. P.Comeset al. AegeanNigella speciation
The main conclusion drawn from the phylogeo-
N. icarica N. arvensis
graphic cpDNA study is that various regional sets of
populations of the Aegean N. arvensis alliance are
N. arvensis geographically isolated and probably on independent
(ssp. brevifolia, evolutionary trajectories. That said, none of its four
Rhodes) constituent species is fixed for a particular cpDNA
haplotype, or uniquely characterized by a haplotype
clade. The same applies to the two selfers N. doerfleri
and N. stricta, which are also nearly fixed for an
ancestral haplotype (A) present in all species of the
alliance except N. icarica (C. Bittkau & H. P. Comes
2004, unpublished data). In general, such cpDNA
haplotype sharing across species boundaries could
N. degenii N. doerfleri
indicate either the retention of ancestral haplotypes
N. stricta or cytoplasmic gene flow/hybridization following
species divergence.
Figure 2. Unrooted neighbour-joining phenogram based on To distinguish between these two possibilities, we
Nei & Li’s (1979) genetic distances among 106 multilocus have undertaken a preliminary survey of amplified
AFLPphenotypesobservedin106plantsfrom42populations fragmentlengthpolymorphisms(AFLPs)inallspecies
of the Nigella arvensis complex, and representing all species
of the complex (except N. carpatha), taking advantage
andsubspeciesexceptN.carpatha,N.arvensisssp.arvensisand
of the fact that such fast evolving markers are
N. degenii ssp. minor. A list containing detailed geographical
predominantly of nuclear origin and also potentially
information on the location of all collection sites and the
suitable for resolving ‘shallow phylogenies’ (Meudt &
numberofindividualssurveyedpertaxon/siteisavailableupon
Clarke 2007). Genetic distance analysis of individual
request. Solid (dashed) branches indicate bootstrap support
valuesabove(below)70%basedon10000replicates.AFLP AFLP phenotypes results in an unrooted network
profiles were generated from total genomic DNA samples (figure 2) in which almost all species of the complex
(Bittkau & Comes 2005) using the AFLP methodology and surveyedareseparatedinclusters,albeitofunresolved
scoring procedure described in Kropf et al. (2006) with two relationships. While a more extensive AFLP survey
EcoRI–MseI primer combinations (E38/M53; E37/M56) that ofapproximately500individualswiththree(insteadof
resultedinatotalof264polymorphicfragments. two) primer combinations is currently underway to
obtainbetter-resolvedspeciesandpopulationrelation-
(becauseofrisingseas)anditsconsequences,including ships (U. Jaros, A. Tribsch & H. P. Comes 2008,
restricted dispersal, drift and population bottlenecks/ unpublished data), two important insights are already
founderevents.InitialevidencethatpresentAegeansea evident from figure 2. First, most nominal species of
barriers keep Nigella populations isolated emerged thecomplexaregeneticallydistinctentities,suggesting
from a survey of polymerase chain reaction-restriction that erratic instances of cpDNA haplotype sharing
fragment length polymorphism haplotype variation of across species boundaries reflect incomplete lineage
cpDNA(whichismaternallyinheritedinNigella)inthe sortingratherthanongoing,interspecifichybridization.
four outcrossing and cross-compatible species of the Second,N.arvensisssp.brevifoliasampledfromRhodes
complex (Bittkau & Comes 2005), henceforth called formsaseparateclusterrelativetoconspecificmaterial
the ‘N. arvensis alliance’. Based on the geographical ofmainlandoriginsurveyed(spp.aristata/glauca).This
distributions of major haplotype clades, as inferred pronounced intraspecific divergence of N. arvensis,
from genealogical (nested clade) reconstructions, this which is also supported by cpDNA data (Bittkau &
studyidentifiedtheEasternand,toalesserextent,the Comes 2005), once more indicates a complete lack of
Western/Southern Aegean Seas as important isolating gene flowacross the East Aegean Seaviz.theStrait of
barrierstoNigelladispersal,ashadlongbeensuspected Marmaris (approx. 18km), which separates Rhodes
for other members of the Aegean flora (Rechinger from the nearby Anatolian coast. It is noteworthy,
1950; Runemark 1969, 1980; Greuter 1979; Strid however, that lack of gene exchange between Nigella
1996). Notably, there was a sharp break in cpDNA populations from either Rhodes (N. arvensis ssp.
haplotypefrequenciesobservedacrosstheEastAegean brevifolia) or the Cyclades (N. degenii) and Anatolia
Sea,i.e.atthe‘Rechinger’sline’(sensuStrid1996),the (N.arvensisssp.glauca)mayalsobeexplained,atleast
phytogeographic borderline between Europe and Asia in part, by reciprocal cross-incompatibility or reduced
Minor. For the first time this testified molecularly to hybrid fertility, respectively, as indicated by experi-
the long-held notion that the East Aegean Sea poses a mentalcrosses(Strid1970,p.117).Thus,evenifseed
strong physical barrier to dispersal in many plants materialfromRhodesortheCycladesmanagestocross
(Greuter1979;Runemark1980;Strid1996),aswellas the East Aegean Sea,the probabilityof gene exchange
for various animals (e.g. Giokas 2000; Fattorini 2002; withresidentAnatolianpopulationsisprobablysmall.
Poulakakis et al. 2003, 2005). Furthermore, the
restricted distribution of a large number of derived
cpDNA haplotypes or clades, on both mainland areas 6.BIOGEOGRAPHY OFAEGEAN NIGELLA
andparticularislands,identifiedtheN.arvensisalliance SPECIATION
as a plant group with low seed dispersal ability and, Knowingaboutthestrengthofageographicalbarrierin
consequently, high susceptibility to genetic drift currentlyrestrictinggeneflowdoes nottellusanything
(Bittkau & Comes2005). aboutitsimportanceinspeciation(Coyne&Orr2004).
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AegeanNigella speciation H. P.Comeset al. 3089
Hence, a crucial question is whether the establishment oflocaladaptationinresponsetolowwateravailability,
of Aegean sea barriers actually caused allopatric which thus would render the two selfers unlikely
vicariant speciation within the N. arvensis complex, candidates for non-adaptive speciation. Given their
i.e. via range fragmentation of a formerly widespread genetic distinctness (figure 2), it also seems unlikely
(pan-Aegean)ancestorofMessiniantomid-Pleistocene that selfing evolved under sympatric conditions as a
origin (Bittkau & Comes 2005). However, considering consequenceofreinforcementtoreducegeneflowfrom
the Late Pleistocenediversification of the complex (see nearby outcrossing populations not adapted to arid
§5a) and in the light of our current understanding of habitats. Rather, we presume that selfing and associ-
post-Messinian sea-level changes in the Aegean (see ated isolating mechanisms (phenological, ecological,
§3b), there are only two probable instances of sea genetic) evolved more or less simultaneously as
barrier-inducedvicariantspeciation,i.e.(i)theoriginof by-products of geographical isolation (Coyne & Orr
N. degenii following the separation of the Cycladic 1999). Experimental crossings and, ideally, sequence
landmass (peninsula) from mainland Greece/Euboea analysesofrelevantgenes(Noor&Feder2006)willbe
(ca 2Ma); and (ii) the probably more recent origin of neededtodeterminethetemporalorderinwhichthese
N. icarica following a post-glacial rise in sea level that multiple isolating mechanisms evolved between out-
separated Ikaria from Samos/Anatolia (ca 125–75ka). crossersandselfers.Importantly,whilemostspeciesof
By contrast, for the remaining island species the N. arvensis complex have allopatric distributions,
(N. doerfleri, N. stricta, N. carpatha), as well as the precludingdirectobservationofreproductiveisolation,
enigmaticN.arvensisssp.brevifolia,thereislittlereason N. doerfleri and N. degenii coexist in the Cyclades
to suspect that rising seaswere required for their origin. (figure 1) without hybridizing (Strid 1970). Evidently,
This is because these taxa mainly (albeit not it is here, in an area of possibly secondary range
exclusively) occur on a group of southern ‘Hellenic overlap, that these multiple isolating factors act
Arc’ islands that became permanently isolated well together to prevent gene flow between these two
before the Late Pleistocene (i.e. Crete, ca 5.5Ma; species, allowingtheircoexistence.
Kithira,Karpathos/Kasos,ca3Ma;Rhodes,ca2.4Ma; To summarize so far, the above data indicate that
see § 3b). In support of this hypothesis, the cpDNA plant speciation in the Aegean Archipelago cannot
data indicate a peripatric origin of N. carpatha through simply be viewed as mainly resulting from vicariant
relatively recent over-sea dispersal from Anatolia (or speciationviahistoricalrangefragmentationbecauseof
Ikaria) to Karpathos (Bittkau & Comes 2005). post-Messinian (Plio-/Pleistocene) rises in sea level.
However, the spatial-temporal origins of N. doerfleri, Thiswastheviewcommonlyheldbyearlierbiosystem-
N. stricta and also N. arvensis ssp. brevifolia are not yet atistsworkingonallopatricplant‘neo-endemics’ofthe
fullyunderstood.Nonetheless,ourcurrentcpDNAand Aegean region (e.g. Snogerup 1967; Stork 1972;
AFLP data (Bittkau & Comes 2005; figure 2) show no Bentzer 1973; Von Bothmer 1974, 1987). In contrast,
evidence of a founder origin of these island taxa from themoleculardatapresentedheresuggestaremarkably
the mainland. Rather, they may constitute remnants of recent (Late Pleistocene) radiation of the Aegean
the formerly widespread ancestral stock from which N. arvensis complex that resulted from a combination
they originated in situ within islands long in existence, of vicariant, (infrequent) peripatric and intra-island
and subsequently dispersed to others to attain their speciation, with the latter process probably facilitated
presently disjunct distributions (figure 1). orevenaccomplishedbyachangeinpollinationsystem
At this juncture it is worth emphasizing that the (selfing).Thatspeciationviafoundereventshadonlya
change fromoutcrossingtopredominant selfing inthe minor role in the group’s history perhaps comes as a
ancestor(s)ofN.doerfleriandN.strictaprobablyhada surprise, but apart from taxon-specific attributes (e.g.
major effect on the origin of these species. Although dispersal ability, genetic incompatibilities) this could
‘selfing’ not necessarily constitutes a reproductive also reflect a migratory situation more typical for
isolating-barrier causing speciation (Coyne & Orr continental (compared with oceanic) island systems,
2004), it nonetheless may contribute to pre-mating wheremostsuccessfulintroductionsofplantdiaspores
barriers between diverging populations and accelerate are generally thought to fail because of niche pre-
the development of intrinsic post-zygotic isolation emption of a resident flora that has long been well
(Fishman & Stratton 2004; Grundt et al. 2006). In adapted to existing habitat conditions (Runemark
fact, the reproductive failure of hybrids in crosses 1969;Silvertown2004;Silvertownet al.2005).
involvingthesetwoselfers(see§4a)mayreflectgenicor More generally speaking, and to compound this
chromosomal incompatibilities that evolved as aresult complexity, it should be recalled that although plant
of reductions in effective population size (because of radiations in continental archipelagos are liable to
selfing) and the fixation of alternate, negatively be partly conditioned by (palaeo)environmental
interacting alleles or chromosomal segments in separ- (extrinsic) factors, such as changes in sea level and
ated populations, often referred to as Dobzhansky– geographical configurations, they may also be pro-
Muller incompatibilities (Orr & Turelli 2001). More- foundly influenced by taxon-specific (intrinsic) attri-
over,bothspeciesshowotherpossibleeffectsofselfing, butes that are thought to influence rates of
including reductions in overall habit and flower size, diversification, including types of pollination,
advanced flowering, as well as successful interisland mechanisms of dispersal, generation time, population
colonization and production of populations in novel, size or hybridization/polyploidization (Coyne & Orr
particularly arid habitats at which the outcrossers are 2004; Ricklefs 2007). Future evaluation of Aegean
absent (see §3b). Hence, the evolution of selfing may plant radiations will thus require not only good
have also led to reproductive isolation as a by-product phylogenetic and phylogeographic data for the
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3090 H. P.Comeset al. AegeanNigella speciation
(a) (b)
20km
(c) (d)
Andros
Tinos
Mikonos
Siros Paros/Naxos
Santorin
Figure3.ReconstructionofthetopographyoftheinsularlandmassofCycladiaattheLGM(ca23–18ka;(a)18ka,(b)14ka,
(c) 12.5ka, (d) 10ka), and the degrees by which it drowned because of rising sea levels towards the end of the Pleistocene
(modifiedfromLambeck(1996)asillustratedinBroodbank(2000)).NamesofislandsfromwhereNigelladegeniipopulations
weresampledforAFLPanalysis(seefigure4,table2)areunderlined.
existence of sister species and accurate molecular landmass of approximately 6000km2, named
clocks to broaden our understanding of the biogeo- ‘Cycladia’ (with several satellite islands), in the place
graphy of plant speciation in the Aegean Archipelago, ofthemodernCyclades.Moreover,refinedcalibrations
but also similar molecular investigations across ofeustaticchangescombinedwithmodellingofcrustal
evolutionarily independent lineages to separate the reboundenabledLambeck(1996)togenerateremark-
effects of historical versus taxon-specific factors on ably precise reconstructions of the topography of
diversification. Finally, further detailed intraspecific Cycladiaandthedegreesbywhichitdrownedtowards
investigations of the population genetic structure of the end of the Pleistocene because of rising seas (ca
Aegean plant species together with experimental 14–10ka;figure3).BythestartoftheHolocene,there
studies are needed to test the strong hypothesis of was a substantial tract of land still present between
Strid (1970) and others (Snogerup 1967; Runemark ‘Greater Paros’ (i.e. the current islands of Paros,
1969, 1980; Stork 1972; Bentzer 1973; VonBothmer Antiparos, Despotikon) and Naxos, but this land
1974,1987)thatallopatricdivergenceviageneticdriftis bridge also rapidly vanished by ca 9ka (Van Andel &
theruleratherthantheexceptionforplantevolutionin Shackleton1982).
theAegeanArchipelago. Our cpDNA population-level survey of Cycladic
N.degenii(Bittkau&Comes2005),althoughsuffering
from low levels of haplotype variation, has revealed
7.INCIPIENT SPECIATION IN THE CYCLADES high levels of genetic differentiation (F ) both
ST
An ideal Aegean plant species with which to test the between sampled islands connected during the LGM
impact of recent population fragmentation on the (i.e. Tinos, Mikonos, Siros, Paros, Naxos), as well
potential for incipient allopatric speciation and as between populations at the species-wide range
genetic/phenotypic divergence via drift is the Cycladic (F Z0.782 versus 0.840). Both results indicate that
ST
endemic N. degenii. The Cycladic region de facto seed flow (NmZ0.139 versus 0.095) is not strong
providesanexcellentsettingforstudyingthehistoryof enough to prevent N. degenii populations from
populationsplittinganditsevolutionaryconsequences, diverging purely by drift (i.e. Nm/1; Wright 1931;
giventhatsea-levelchangesintheareasincetheLGM Slatkin 1985). To further investigate the species’
(ca !23–18ka) are well documented (Van Andel & history of population splitting and divergence in the
Shackleton 1982; Lambeck 1996; Perissoratis & Cyclades, we have undertaken a survey of AFLP
Conispoliatis 2003). Starting with the LGM, there variation in 110 individuals, representing six Cycladia
wasamajordropinsealevelthatcreatedalargeinsular populations (ssp. barbro: Tinos, Mikonos; ssp. jenny:
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AegeanNigella speciation H. P.Comeset al. 3091
Table2.LocationofsitesusedinthepresentAFLPstudyforNigelladegeniidistributedacrosstheCyclades,andsummaryof
AFLPvariationforatotalofsevenpopulations.VariationisdescribedbytheproportionofAFLPmarkers(‘loci’)polymorphic
(PLP)andNei’s(1973)expectedheterozygosityH (or‘genediversity’,withF assumedtobezero)calculatedbytheprogram
e IS
FDIST(Beaumont&Nichols1996).
N.degeniitaxon localitya latitude(N) longitude(E) PLP H n
e
ssp.barbro Tinos,EofAgiosFokasbeach 3783105400 2581301100 0.342 0.110 14
Mikonos,Panormosbeach 3782802700 2582104200 0.361 0.109 18
ssp.jenny Siros,nearKokkinabeach(Finikas) 3782304400 2485201600 0.390 0.152 19
ssp.degenii Paros1,SofCapeKorakas 3780805200 2581302000 0.417 0.128 15
Paros2,SofLefkes 3780300800 2581204500 0.426 0.155 18
Naxos,WofHimaros 3780303600 2582703900 0.333 0.110 13
Santorin,SofFira 3682404000 2582601500 0.491 0.173 13
aAllcollectionsbyC.Bittkau.Seefigure4(inset)forgeographicallocation.
Naxos
Tinos
Mikonos
Siros
Naxos
Paros Paros1
nii
Santorin ge
e
d
p.
s
Paros2 s
62
68
Santorin
y
96 Siros nn
e
p. j
s
s
59
Mikonos
o
r
b
r
a
b
Tinos p.
s
s
100 57
Figure 4. Neighbour-joining analysis of 110 multilocus AFLP phenotypes observedin 110 plants from sevenpopulations of
Nigella degenii from the Cyclades (inset) based on Nei & Li’s (1979) genetic distances (see table 2 for locality information).
Intermingled individuals from populations Paros1, Paros2 and Naxos are highlighted (dark, medium and light grey,
respectively).Bootstrapvalues(O50%)basedon10000replicatesareshownabovebranches.AFLPprofilesweregenerated
fromtotalgenomicDNAsamples(Bittkau&Comes2005)accordingtoScho¨nswetteretal.(2002)withslightmodifications,
and using two EcoRI–MseI primer combinations (ECACA/MCCAGC; ECACC/MCCAGA) that resulted in a total of 108
polymorphicfragments.
Siros; ssp. degenii: Paros1/2, Naxos), plus one ssp. recognizing five population clusters corresponding to
degeniipopulationfromthevolcanicislandofSantorin/ Tinos, Mikonos Siros,Santorin and Paros (1/2)/Naxos
Thera, which has been isolated from Cycladia at least (figure5).Moreover,therewasnosignificantassociation
since the last interglacial (Snogerup 1967; Greuter between genetic and geographical distances of these
1979; Sfenthourakis 1996; see table 2 and inset of populations(rZ0.249,Manteltest,pZ0.177).Thislack
figure4forsamplingsites).Geneticdistanceanalysisof ofisolation-by-distanceinconjunctionwithpronounced
these individuals results in an unrooted neighbour- population subdivision (F Z0.290; figure 5) once
ST
joiningphenogram(figure4)inwhichmostindividuals moresuggeststhatgeneticdrifthasbeenofmuchgreater
cluster according to their populations except for historical importance in these Cycladic populations
those from Paros (1/2) and Naxos, which cannot be compared with recurrent gene flow (Hutchison &
clearly distinguished. Bayesian analysis of population Templeton1999).
structure as implemented in the program Structure Despite low internal bootstrap support, the tree
v. 2.1 (Pritchard et al. 2000) confirms this pattern by topologyshowninfigure4isstrikinglycongruentwith
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3092 H. P.Comeset al. AegeanNigella speciation
1 2 3 4 5 4
100%
90% 1 = Mikonos
80%
2 = Tinos
70%
60% 3 = Siros
50% 4 = Paros1/2 + Naxos
40%
5 = Santorin
30%
20%
10%
0%
Figure5.HistogramofSTRUCTUREassignmenttestforsevenCycladicNigelladegeniipopulations(110individuals)basedon108
polymorphicAFLPfragments.Eachverticalbarrepresentsanindividualanditsassignmentproportionintooneoffive(white
to black coloured) population clusters (K). After a burn-in period of 200000 iterations, 10 independent runs of KZ1–7
were performed at 106 Markov chain Monte Carlo samplings. The model with KZ5 explained the data as satisfactorily
as models with KZ6 or 7 (showing similarly high log-likelihood values), whereby the latter did not further improve the
resolutionamongthepopulationsParos1,Paros2andNaxos(datanotshown).
the temporal order in which Cycladia fragmented As such, the species reiterates the major evolutionary
(figure 3), with Tinos and Mikonos separating first and biogeographic processes of speciation as invoked
(14–12.5ka), followed by Siros (12.5–10ka), and for theentireN.arvensiscomplex,albeitatatimescale
Paros and Naxos last (10–9ka). Under this scenario, probably much shorter than that required for most
the high genetic similarity viz. admixture observed speciation in this plant group. Clearly, the population
between populations from these latter islands would demographic history of N. degenii remains to be
reflect recent common ancestry rather than post- explored morefully, ideally with multi-locuscoalescent
divergence gene exchange. While we cannot presently methods at the DNA sequence level (Majoram &
distinguishbetweenthesetwopossibilities(butsee§8), Tavare´ 2006),andwiththetargetofdirectlyestimating
amoreintriguing issuetobesolvedistheoriginofthe times since population isolation, population-size
Santorin population of N. degenii, which does not changes at the time of divergence and post-divergence
conform to the expectations of a recent colonization rates of gene flow. Inferring such key demographic
(e.g. Carstens et al. 2005; Kropf et al. 2006). Instead parameters in an Aegean plant species such as
thispopulationgroupsnexttotheParos/Naxoscluster N. degenii, occupying a patchwork of approximately
rather than being nested within this group (figure 4) 20 islands in the Cyclades, would provide an excellent
and shows elevated rather than reduced levels of test case for the rapidly expanding field of ‘divergence
genetic diversity (table 2). Together, this suggests that population genetics’ (Hey & Nielsen 2004, 2007;
an over-sea dispersal event occurred from the Paros/ Dolman & Moritz 2006; Marjoram & Tavare´ 2006).
NaxosareatoSantorin,andthattimewassufficientfor However, whether the magnitude of genetic diver-
geneticdiversitytoevolveinthecolonizedarea,andto gence among populations within a species or between
erase any pattern of nestedness because of the speciesmaybeconsideredanindicatorof,respectively,
accumulation of de novo mutations and/or the effects incipient and full speciation is likely to depend on the
of continued lineage sorting (Avise 2000). Hence, if species concept invoked (Baum 1992; Avise 2000;
our inferred times and orders of Cycladia population Hey2001;Coyne&Orr2004).Inanyevent,basedon
splittingarecorrect,andbarringinsufficientpopulation our current molecular (AFLP) evidence (figure 2),
sampling, N. degenii must have dispersed to Santorin the two selfers (N. doerfleri and N. stricta) and most
shortly before the Paros/Naxos mega-island broke up speciesoftheoutcrossingN.arvensisalliancedidevolve
(ca 9ka). In turn, this would raise the intriguing as independent and coherent gene pools (except
possibility that the massive eruption of the Thera N.arvensis).However,whereastheselfersaccumulated
volcano in the mid-second millennium BC (Heiken & sufficient reproductive isolation barriers (inter-se and
McCoy1984)didnoteradicateN.degeniionSantorin towards the alliance), species of the latter group
(seeThorpeetal.2008,forasimilarscenarioinLesser remained interfertile (see §4b). That said, closer
AntilleanAnolislizards). scrutinyofStrid’s(1970)crossingdatafor thealliance
reveals various degrees of partial hybrid sterility both
at the inter- and intraspecific levels. While pending
8.CONCLUSIONS AND FUTURE DIRECTIONS better-resolved species and population relationships,
The geographical distribution of intraspecific genetic it is tempting to speculate that the magnitude of
(cpDNA, AFLP) variation in N. degenii from the such partial (intrinsic post-zygotic) reproductive
Cycladesisbroadlyconsistentwithapuredrift/isolation isolation between pairs of species or populations will
model. In other words, historical, non-equilibrium increase with genetic distance, as would be expected
samplingprocessesfollowingpost-glacialfragmentation forDobzhansky–Muller incompatibilities(see §6) that
of Cycladia or (rarely) long-distance colonization have evolvebecauseofintragenomicconflictsasby-products
indeed been the primary determinants of population of the divergence of genomes in allopatry and via drift
divergence across these islands. These patterns of (Price & Bouvier 2002; Moyle et al. 2004; Bolnick &
intraspecific genetic divergence therefore may render Near 2005; Burt & Trivers 2006; see Mallet 2008;
N. degenii at an incipient stage of allopatric speciation. Cozzolino & Scopece 2008). Also, it would be worth
Phil.Trans.R.Soc.B(2008)