The Causes of Evolutionary Radiations in Archipelagoes

13 Pages·2007·0.4 MB·English

vol. 169, no. 3 the american naturalist march 2007 (cid:1)
The Causes of Evolutionary Radiations in Archipelagoes:
Passerine Birds in the Lesser Antilles
Robert E. Ricklefs1,* and Eldredge Bermingham2,†
1.DepartmentofBiology,UniversityofMissouri,St.Louis, Keywords:adaptiveradiation,allopatry,colonization,LesserAntilles,
Missouri63121; speciation,sympatry.
2.SmithsonianTropicalResearchInstitute,Apartado2072,Balboa,
RepublicofPanama
Amongbirds,evolutionaryradiationswithinarchipelagoes
SubmittedMay17,2006;AcceptedOctober10,2006; include the Darwin’s finches (Geospizinae) of the Gala´-
ElectronicallypublishedJanuary17,2007
pagos(Lack1947;Bowman1961,1963;Grant1986;Burns
etal.2002)andthehoneycreepers(Drepanidinae)ofHa-
Onlineenhancement:appendix.
waii (Amadon 1950; Pratt 1979; Fleischer and McIntosh
2001; James 2003). Birds are relatively mobile, and phy-
logenetic analysis of avian sister lineages provides no in-
dication of speciation within islands as small as 1,000–
abstract: Toinvestigatewhysomelineagesundergoevolutionary 10,000 km2 (Fleischer and McIntosh 2001; Ricklefs and
radiation,wecomparethepasserineavifaunasoftheHawaiianand Bermingham 2001; Burns et al. 2002). Therefore, accu-
Gala´pagos archipelagoes, which have supported well-knownradia- mulation of species belonging to a single clade on indi-
tionsofbirds,withthoseoftheLesserAntilles,whichhavenot.We vidual islands within an archipelagois thoughttoinvolve
focus on four steps required for the buildup of diversity through
genetic differentiation of island populations in isolation
allopatricspeciationandsecondarysympatry:geneticdivergencein
followedbyreinvasionofoneislandbyasisterpopulation
isolation,persistenceofislandpopulations,recolonizationofsource
from another island (Lack 1947; Mayr 1963; Grant 1998;
islands,andecologicalcompatibilityinsecondarysympatry.Analysis
CoyneandPrice2000;GrantandGrant2002).Intheevent
ofgeneticdivergenceamongislandpopulationsintheLesserAntilles
that such secondarily sympatric populations do not in-
reveals evidence of both prolonged independent evolutionandre-
expansion of differentiated island populations through the archi- terbreed,theyareconsideredseparatespecies(Mayr1963;
pelagobutlittleevidenceofsecondarysympatryofdivergentgenetic Templeton 1989; Coyne and Orr 2004).
lineages. Archipelagoes with high rates of colonizationfromconti- Not all archipelagoes have supported evolutionaryradi-
nental or nearby large-island sources might fail to promoteevolu- ations.Inthecaseofbirds,neithertheLesserAntilles(Bond
tionaryradiationsbecausecolonistsfillecologicalspaceandconstrain 1956,1963,1979)northeNewHebrides(Vanuatu)(Med-
diversification through competition.However,morphologicalanal- way and Marshall 1975; Diamond and Marshall 1976,
ysisdemonstratedsimilardivergencebetweenallopatricpopulations
1977a), for example, are regarded as crucibles of species
in species in Hawaii, Gala´pagos, and the Lesser Antilles, although
production. Instead, avian taxa inhabiting these archipela-
therateofdivergencebetweensecondarilysympatricspeciesevidently
goes represent primarily separate invasions from nearby
is more rapid in Hawaii andtheGala´pagos.Alternatively,endemic
continentalorlarge-islandsourcesofcolonists(Bond1963;
buildup of diversity might be facilitated by the relative absence of
Lack1976;RicklefsandBermingham2001).Althoughmany
pathogensinHawaiiandGala´pagosthatotherwisecouldpreventthe
secondarysympatryofpopulationsowingtodisease-mediatedcom- of these taxa are old and have been described as endemic
petition. species and genera, they have generally not diversified in
the sense of producing sympatric daughter species.
Althoughevolutionaryradiationisunderstoodingen-
* Addressforcorrespondence:DepartmentofBiology,UniversityofMis-
eraloutline(GivnishandSytsma1997;Grant1998;Grant
souri,8001NaturalBridgeRoad,St.Louis,Missouri63121-4499;e-mail:
and Grant 1998; Schluter 2000), factors that promoteor
[email protected].
retard diversification are not. In this article, we use de-
† Mail originating in the United States should be addressedto Unit0948,
APOAA34002-0948;e-mail:[email protected]. tailed phylogeographic analyses of Lesser Antillean birds
Am.Nat.2007.Vol.169,pp.285–297.(cid:1)2007byTheUniversityofChicago. (Ricklefs and Bermingham 1999, 2001, 2004) to explore
0003-0147/2007/16903-41843$15.00.Allrightsreserved. factorsthatpotentiallycouldconstraintheallopatricfor-
286 The American Naturalist
Figure1:MapsoftheNewHebrides,LesserAntilles,Hawaii,andGala´pagosarchipelagoestothesamescaleillustratethegeneralsimilarityofisland
sizeanddistance.
mation of new species and their secondary sympatry threshold, and (iii) secondary sympatry does not occur
withinarchipelagoes,whichwedefineasanevolutionary owing to too little movement between islands.
radiation.Weavoidtheterm“adaptiveradiation”tofore- Evolutionary radiations of birds on the Gala´pagos and,
stall judgment concerning phenotypic or ecological di- especially, Hawaiian archipelagoes have at least partially
versification. Although evolutionary radiations charac- filledtheecologicalspaceoccupiedbymorephylogenetically
terize the diversification of life everywhere, islands diverse assemblages of species on less remote islands and
provide suitable laboratories for studying this phenom- continents (Schluter 1988; Burns et al. 2002; Lovette et al.
enonowingtothediscretenatureofpopulationsandthe 2002).Thissuggeststhatevolutionaryradiationsoccurmost
clear distinction between allopatry and sympatry. Fur- readilywhereecologicalspaceisavailable,conspicuouslyon
thermore, evolutionary radiations within oceanic archi- newand/orremoteislands(Schluter1988).Toaddressthis
pelagoes of volcanic origin have a clearly recognizable issue, we use morphological diversity as a proxy for eco-
beginning, which is a colonization event from outside. logicaldiversitytodeterminewhethersympatryisassociated
Evolutionary radiation leading to the co-occurrence of with a minimum level of ecological divergence.
descendantspeciesonthesameislandcanoccuronlywhen We find that none of the requirements 1 through3for
four requirements for allopatric speciation are met (see, allopatric speciation appears to limit evolutionary radia-
e.g., Allmon 1992; Mayr and Diamond 2001; Newton tion in the Lesser Antilles. Step 4, the achievement of
2003): (1) dispersal between islands must be sufficiently ecological compatibility, might be hindered in the Lesser
low to permit genetic divergence, (2) island populations Antilles by the lack of ecological opportunity owing to
mustpersistlongenoughtodivergegeneticallytoapoint the ecological diversity of colonizing lineages or by host-
ofincompatibilityresultingfromeitherprematingorpost- specific pathogens that prevent co-occurrence.
mating isolating mechanisms, (3) isolated populations
must occasionally recolonize other islands, and (4) newly
sympatric sister taxa must be reproductively isolated and Material and Methods
ecologically compatible.
The Archipelagoes
Wefirstdeterminewhetherdifferencesintheoccurrence
of evolutionary radiations among four similar archipela- We initially compare four tropical archipelagoes that fea-
goes have statistical validity. We then use genetic diver- ture similar numbers of large islands and distances be-
gencebetweenislandpopulationsofpasserinebirdsinthe tween islands, with the exception that the Gala´pagos Ar-
Lesser Antilles to evaluate requirements 1 (isolation), 2 chipelago is more compact than the other three (fig. 1).
(persistence), and 3 (recolonization). Specifically, we test TheGala´pagosIslandsdifferfromtheotherislandgroups
hypotheses concerning factors that might prevent evolu- ecologicallyintherelativearidityoflow-elevationhabitats
tionaryradiations,namely,that(i)continuingdispersalof and the strong influence of ElNin˜o–SouthernOscillation
individuals prevents genetic divergence of island popula- events on climate (Colinvaux 1984). Humans have had a
tions in archipelagoes, (ii) island populationsdonotper- profound effect on the avifaunas of each groupofislands
sist long enough to diverge genetically to a speciation (Pregill andOlson 1981; Olson andHilgartner1982;Pre-
Evolutionary Radiations in Archipelagoes 287
gill et al. 1988, 1994; James and Olson 1991; Steadman and Pratt (1979), Berger (1981), and James and Olson
1995,2006;SteadmanandRolett1996;PregillandCrother (1991) for the Hawaiian Islands. A list of the colonizing
1999; Steadman et al. 2002; Steadman and Martin 2003), lineages producing the contemporary avifauna of each of
probably least in the Gala´pagos Islands, which currently theislandgroupsisprovidedintheappendix,availablein
supports a small human population distributed among the online edition of the American Naturalist.
fourofthelargerislandsandwhichhadnopre-European
history of colonization (Perry 1984). Human-caused ex-
tinctions have reduced the diversity and distributions of
Genetic and Morphological Analyses
somegroupsofislandbirds(Steadman1995)butprobably
have caused the extinction of few passerines intheLesser Geneticdivergencebasedon842basepairsofthepartial-
Antilles and New Hebrides. Indeed, the clearest example ly overlapping mitochondrial ATPase 6 and ATPase 8
of evolutionary radiation in island passerine birds comes protein-coding genes has been reported in previous
from the Hawaiian archipelago, which has suffered the publications;materials,methods,andGenBankaccessions
greatest loss of island populations and species. can be accessedthroughtheoriginalarticles(e.g.,Lovette
Theislandgroupsareallprimarilyvolcanicinoriginbut et al. 1998, 1999a, 1999b; Hunt et al. 2001). Details, in-
differ in their relative ages, the Lesser Antilles (∼20 Ma; cluding GenBank submission numbers, are provided in
Donnelly 1988, 1989; Perfit and Williams 1989; Iturralde- the electronic supplementary materials to an article by
Vinent and MacPhee 1999) and New Hebrides (∼20 Ma, Ricklefs and Bermingham (2001; http://www.sciencemag
butwithextensiveareaonlyafter2Ma;Mallick1975)being .org/cgi/content/full/294/5546/1522/DC1).
olderthanthepresent-dayGala´pagos(atleast3.3Ma;Cox Morphologicalanalysesarebasedonthemeansoflog -
10
1983; Hall et al. 1983; Simpkin 1984; Sinton et al. 1996; transformedmeasurementsforeachspecies,includingto-
Hoernle et al. 2000) and the main Hawaiian islands (∼5.1 tal length, wing, tarsus, middle toe, tail, and the length,
Ma;ClagueandDalrymple1987;CarsonandClague1995). width, and depth of the bill (Ricklefs and Travis 1980).
HawaiiandtheGala´pagos,3,800and850km,respectively, Themorphologicalvariablesweresubjectedtoaprincipal
from North and South America, are considerably farther components analysis (PCA) of the variance-covariance
from continental sources of colonization than the Lesser matrix of the log-transformed values (Ricklefs and Travis
AntillesandNewHebrides.Grenada,inthesouthernLesser 1980;LegendreandLegendre1998).Morphologyprovides
Antilles, is approximately 150 km from the coast of Vene- a reasonable assessment of foraging substrate, feeding
zuela. Although Espiritu Santo in the New Hebrides is movements, and prey size (e.g., Miles and Ricklefs 1984;
roughly 380 km from New Caledonia and 1,000 km from Miles et al. 1987). Pairwise distance (D ) between two
ij
thecoastsofAustraliaandNewGuinea,alargenumberof species (i and j) in morphologicalspace wascalculatedas
colonistshavereachedtheislandsfromthewestbywayof the Euclidean distance based on n measurements, thatis,
stepping-stone islands.
(cid:1)
(cid:2)n
D p (x (cid:1)x )2,
The Birds ij ik jk
kp1
We restrict this analysis to passerine birds (songbirds, or
perching birds: order Passeriformes) because these com- where x and x are the values for measurement k for
ik jk
prise a well-characterized monophyletic group with rea- species i and j, respectively. For each species, the smallest
sonablyuniformbiologicalattributesandbecausemostof distance to another species was designated as the nearest
the species from the Lesser Antilles for which we have neighbordistance(NND;RicklefsandTravis1980).When
estimatedgeneticdistancesarepasserinebirds.Inaddition, the nearestneighbordistancewasbasedonalleightmea-
the conspicuous radiations of birds in the Gala´pagos Is- surements,itwasdesignatedNND.Inothercomparisons
8
lands (the Darwin’s finches: subfamily Geospizinae) and based on fewer measurements, generally taken from lit-
the Hawaiian Islands (the honeycreepers: subfamily Dre- erature sources (see “Results”), pairwise distances and
panidinae)arepasserines;comparedtootherislandbirds, nearestneighbordistancesweredesignatedD andNND .
n n
relatively few passerines have become extinct following Because each measurement contributes approximately
human occupation. equally to the total Euclidean distance, the ratio of the
Taxonomyanddistributionsofpasserineswereobtained expected distances with y and z measurements, which is
from Bond (1956, 1979), the American Ornithologists’ (y/z)1/2,providesabasisforcomparison.Allstatisticalanal-
Union (1998), and Raffaele et al. (1998) for the Lesser yses were performed with SAS software (SAS, Cary, NC)
Antilles;DiamondandMarshall(1976,1977a)fortheNew or with the PopTools add-in to Excel (http://www.cse
Hebrides; Harris (1973) for the Gala´pagos Archipelago; .csiro.au/poptools/) and are described in “Results.”
288 The American Naturalist
Results Accordingly, we examine the birds of the Lesser Antilles,
the only regional assemblage of passerines studiedfroma
The Frequency of Evolutionary Radiations
DNA-based phylogeographic perspective (Seutin et al.
The number of independent colonizations to an archi- 1993,1994;Lovetteetal.1998,1999a,1999b;Ricklefsand
pelago is associated with the frequency of evolutionary Bermingham 1999, 2001; Hunt et al. 2001; Miller et al.,
radiationsandlevelsofendemismwithintheislandgroup forthcoming), in terms of the four requirements for evo-
(table 1). In the Hawaiian Islands, one ancestral stock of lutionary radiation: genetic divergence in allopatry, per-
cardueline finch gave rise to at least 35 historical species, sistence of diverging populations, opportunity for sec-
including 15 species of honeycreepers on the island of ondary sympatry, and ecological compatibility of sec-
Hawaii alone (Amadon 1950; Pratt 1979), and many ad- ondarily sympatric populations.
ditionalformsthatarenowextinct(JamesandOlson1991;
James 2003). In the Gala´pagos Islands, a single ancestral
Step 1: Opportunity for Genetic Divergence
stockproducedamonophyleticcladeof13speciesofDar-
win’sfinches,withupto11speciesonasingleisland(Lack DifferentiationofislandpopulationsofbirdsintheLesser
1947; Harris 1973; Grant 1986; Petren et al. 1999; Satoet Antillesissuggestedbysubspecificnamesassignedtomany
al. 1999), although the definition of species within this of these (Bond 1956). Gaps in the distributionsofseveral
group is somewhat uncertain (Zink 2002) and hybridi- species(Bond1956;RicklefsandCox1972)furthersuggest
zation between named species is not uncommon (Grant thatindividualsofsomespeciesmovebetweenislandstoo
and Grant 1998). In the Lesser Antilles, the only evolu- infrequently to recolonize islands left unoccupied follow-
tionary radiation among passerine birds comprises four ingextinction,letalonetopreventgeneticdifferentiation.
endemicspeciesofthrashers(Mimidae;Huntetal.2001), RecentmolecularphylogeneticstudiesofbirdsintheLes-
all four of which coexist on the islands of St. Lucia and ser Antilles (Seutin et al. 1993, 1994; Lovette et al. 1998,
Martinique. No evolutionary radiations are apparent in 1999a,1999b;RicklefsandBermingham1999,2001;Hunt
the New Hebrides (Diamond and Marshall 1976). etal.2001)showthatgeneticdivergencebetweenallopatric
The current passerine avifaunas of the Hawaiian and populations is common, especially for endemic Antillean
Gala´pagos archipelagoes have each been derived from six taxa. We have surveyed 25 monophyletic lineages of pas-
colonization events and together have produced at least serine birds within the Lesser Antilles, 22 of which were
62 historical species, of which 97% are endemic (table 1; represented by two or more island populations. Of these,
also see appendix). In the New Hebrides and Lesser An- eight exhibit mitochondrial (ATPase 6, 8) nucleotide di-
tilles, 24 and 34 colonization events have together pro- vergencesbetweenatleastonepairofislandsgreaterthan
duced 61 species, of which only 33% are endemic. Dif- 0.5%, which exceeds most (197%) within-populationge-
ferencesintheproportionsofendemicgeneraandspecies neticdistances.Basedonestimatedcoalescencetimes(see
between these two sets of archipelagoes are highly signif- “Step 3: Recolonization Ability”), the expected level of
icant (Gp22.4, P!10(cid:1)5 and Gp63.5, P!10(cid:1)14, re- genetic diversity in mtDNA within island populations is
spectively). about 0.1% nucleotide divergence, which is close to the
In the New Hebrides and Lesser Antilles, one of 58 median observed in 104 island populations of 32 species
colonizationeventsrepresentedamongextanttaxaresulted (Ricklefs and Bermingham 2001; R. E. Ricklefs and E.
in a modest evolutionary radiation. In the Hawaiian and Bermingham,unpublisheddata).Sevenspecieshadinter-
Gala´pagos archipelagoes, three of 12 colonization events island divergences exceeding 1%, and five exceeded 2%.
producedradiationsthatbuiltoveralldiversitytoapprox- Eleven of 14 species with maximum interisland diver-
imately the levels of the less remote archipelagoes. If we gences less than 0.5% have conspecific populations in
assumethatthecolonizinglineagesareindependent,then, northernSouthAmericaortheGreaterAntilles.Evidently,
from a statistical standpoint, one of 58 and three of 12 these are either recent colonists to the Lesser Antilles
differ significantly (Gp5.6, Pp.018). (RicklefsandBermingham2001)orspecieswithcontinu-
BecauseofavifaunalsimilaritiesbetweentheLesserAn- inghighlevelsofmovementbetweensourceareasandthe
tilles,Gala´pagos,andHawaii(seeappendix),thepresence Lesser Antilles and among islands within the archipelago
or absence of evolutionary radiations is unlikely to be (Johnson et al. 2000; Cherry et al. 2002). The otherthree
related to particular characteristics of passerine colonists speciesareendemicLesserAntilleantaxawitheitherrecent
of archipelagoes. Specifically, near relatives of the finches secondary phases of colonization within the archipelago
and thrushes that gave rise to the evolutionaryradiations or recent high levels of gene flow.
in the Gala´pagos and Hawaiian archipelagoes are present Five of 13 of the endemicLesser Antilleantaxa(12.0%
in the Lesser Antilles (Tarr and Fleischer 1995; Burns et divergence from source) that we have surveyed exhibit
al. 2002; Lovette et al. 2002; Miller et al., forthcoming). interisland divergences within the range of 2%–8%.Such
Evolutionary Radiations in Archipelagoes 289
Table 1: Characteristicsof the describedpasserinefaunas of four archipelagoesa
Characteristic LesserAntilles New Hebrides Gala´pagos Hawaii
Total area (km2) (Stattersfieldet al. 1998) 6,300 13,000 8,000 16,300
Maximumelevation(m) 1,500 1,800 1,700 4,200
Nearestcontinent(distance,km) South America Australia South America North America
(150) (1,000) (850) (3,800)
Number of colonizations 34 24 6 6
Number of genera (endemic) 30 (8) 18 (1) 8 (4) 16 (14)
Number of species(endemic) 37 (16) 24 (4) 21 (19) 41 (41)
Maximumnumber of specieson one island 28 22 16 21
Radiations 1b 0 1c 2d
Number of taxa produced 4 0 13 35e
a Sourcesofdata:LesserAntilles(Bond1956,1979;AmericanOrnithologists’Union1998;Raffaeleetal.1998);NewHebrides(DiamondandMarshall
1976,1977b);Gala´pagos(Harris1973);Hawaii(Pratt1979;Berger1981;JamesandOlson1991).
b Theendemicthrashers(Sturnidae:Mimini;Huntetal.2001);asecondradiationresultedintwosympatricspeciesofthenonpasserine,hummingbird
(Trochiliformes)genusEulampis(E.BerminghamandR.E.Ricklefs,unpublisheddata).
c TheGala´pagosfinches(Geospizinae)derivedfromacontinentalorWestIndianemberizidcolonist(Fringillidae:Emberizinae;Burnsetal.2002).
d TheHawaiianhoneycreepers(Drepanidinae)derivedfromacarduelinefinch(Fringillidae:Carduelinae)plustheHawaiianthrush(Omao,belonging
totheAmericangenusMyadestes)representedbytwospeciesontheislandofKauai(FleischerandMcIntosh2001;Lovetteetal.2002).
e Thenumberofspeciesdescribedfromlivingmaterial,13ofwhichareextinct;atleast24additionalfossiltaxahavebeendescribed(James2003).
levels are characteristic of congeneric and, in manycases, expandedandolderendemicLesserAntilleantaxa,Ricklefs
sympatric North American species of passerine birds and Bermingham (1999) estimated that individual island
(4.4%(cid:2)1.9% SD, np11; Seutin et al. 1993; 5.1%(cid:2) populationsdisappearatanaveragerateofabout0.5Ma(cid:1)1
3.0%SD,rangep0.4%–10.9%,np35;KlickaandZink onthelargerislandsoftheLesserAntilles.Noislandgaps
1997; also see Avise 1994; Tarr and Fleischer 1995; Zink have appeared among species that have spread through
1996; Lovette et al. 2002; Weir and Schluter 2004). These thearchipelagomorerecentlythan1Ma.Accordingly,the
levels are also consistent with the average divergence in average life span of a population on the larger islands in
mtDNA sequences of 3%–4% observed between species theLesserAntillesappearstobeatleast2Ma.Thus,pop-
ofHawaiianhoneycreepers(TarrandFleischer1993,1995; ulation persistence appears not to limit the potential for
FleischerandMcIntosh2001;Lovetteetal.2002)andthe secondary sympatry, at least not in the Lesser Antilles.
maximum divergence in mtDNA sequences between spe-
cies of Darwin’s finches in Gala´pagos (about 4%; Sato et
al. 1999). Thus, although many taxa are widespread
Step 3: Recolonization Ability and the Paucity of
throughout the Lesser Antilles, genetic divergenceamong
Secondary Sympatry in the Lesser Antilles
a number of conspecific populations is similar to levels
exhibited by sympatric species found on islands in the
Secondary sympatry depends on the recolonization of is-
Gala´pagos and Hawaiian archipelagoes.
landsfollowingperiodsofgeneticdivergence.Of13species
ofold(12%sequencedivergence)LesserAntilleanlineages
for which we have estimated colonization timesbasedon
Step 2: Persistence of Island Populations
molecular phylogenies (Ricklefs and Bermingham 2001),
The presence of highly differentiated island populations seven (54%) show secondary expansion with genetic di-
suggests that some species persist long enough forphases vergences of less than 1% between at least some pairs of
ofsecondarycolonizationwithinthearchipelagotoresult island populations. If one assumes that 1% sequence di-
in more than one taxon of an autochthonous clade on a vergence is equivalent to 0.5 Ma (Lovette 2004), thisrep-
singleisland(i.e.,anevolutionaryradiation).Nonetheless, resentsanexponentialrateofsecondaryexpansionof1.23
gaps in the distributionofoldertaxaindicatethatextinc- per taxon per Ma (i.e., (cid:1)ln[0.54]/0.5 Ma). If periods of
tion may be a significant process in the Lesser Antilles secondary expansion occurred at random (i.e., exponen-
(Ricklefs and Cox 1972; Ricklefs and Bermingham1999). tially)overtime,thisratewouldcorrespondtoanaverage
Gaps occur mostly in species with interisland genetic di- waiting time of 1.6% mtDNA genetic differentiation be-
vergences exceeding 2%. Extinction of individual island tween colonization phases,with10%ofwaitingtimesex-
populations reduces the probability that colonizationwill ceeding3.7%mtDNAdifferentiation.Thus,opportunities
result in secondary sympatry. forsecondarysympatryofgeneticallydivergentsisterpop-
Based on comparisons of the distributions of recently ulations appear to be reasonably high. Yet, only among
290 The American Naturalist
the endemic Mimidae have expansions resulted in sym- and the yellow warbler Dendroica petechia) exhibit rela-
patric sister taxa. tivelydivergenthaplotypesonsingleislands,suggestiveof
Secondary sympatry might be absent from the Lesser the mixing of previously isolated populations (fig. 2, case
Antilles because secondary expansions (i) originate from VI; see appendix for details).
single-island endemics, (ii) swamp sister populations on If secondary sympatry occurred at a time in the past
other islands through hybridization, or (iii) exclude, or longer than the coalescence time of the population, co-
succumbtoexclusionby,sistertaxaremainingoninvaded existing differentiated lineages would probably have been
islands. lost by drift, leaving a single one of the lineages in the
Expansionbysingle-islandendemics.Evidenceformech-
contemporarypopulation.Becauselineagesarelostatran-
anism (i) would be obliterated by the expansion itself.
dom,however,evidenceofsecondarysympatrymightap-
However, single-island endemics are rare in the passerine
pearasgeographicallyunordereddistributionsofdivergent
fauna of the Lesser Antilles. Only three of 16 endemic
lineagesamongislands(fig.2,caseV).Theonlyplausible
Lesser Antillean passerine lineages are currentlyrestricted
case for geographically unordered divergent lineages
to a single island: Melanospiza richardsoni and Leucopeza
within a species among passerine birds of the Lesser An-
semperionSt.LuciaandCatheropezabishopionSt.Vincent
tillesisthetrembler(Cinclocerthiaruficauda).Inthisspe-
(fig.2,caseI).Wecalculatedthat62%–91%ofsecondarily
cies, a single St. Vincent individual was closely related to
expanding populations within the core Lesser Antillean
individualsonDominica(dp0.00%);theinterveningis-
islandswouldencountersisterpopulationsonatleastone
landpopulation(CinclocerthiagutturalisonSt.Lucia)was
other of these islands (see appendix).
4.3%divergentfrombothofthese.Webelieveitispossible
Hybridizationandswamping.Mechanism(ii)wouldper-
thatC.ruficaudawasintroducedtoSt.VincentfromDom-
tainifacolonizingpopulationanditsresidentsisterpop-
inica during the nineteenth century (see appendix).
ulation on an island were behaviorally and genetically
compatible.Ifthesecondaryexpansionwererelativelyre- Exclusionofresidentbycolonist.Mechanism(iii),namely
cent, that is, within the coalescence time of the resulting competitive exclusion of resident populations by a colo-
population, secondary colonization could be recognized nizing, reproductively incompatible sister lineage, would
in principle by the coexistence of divergentlineagesfrom obliterate the evidence of its having occurred, as in the
more than one island. Few mtDNA genetic distances caseofmechanism(i),leadingattheextremetothewide-
within island populations exceed 0.005, or 0.5%. Among spreaddistributionofasingleendemiclineage(fig.2,case
well-sampled,widespreadLesserAntilleanpasserines,only III).OnlytheendemicLesserAntilleanbullfinch(Loxigilla
two species (the pearly eyed thrasher Margarops fuscatus, noctis)exhibitssuchadistribution,whichalsocouldhave
Figure2:Schematicdiagramofthedistributionofdivergentlineagesacrossislands(geography)accordingtoseveralscenarios.Shadedbarswithin
eachscenariorepresentdifferenthaplotypes.Thehorizontalextentofeachbarrepresentsthegeographicdistributionofthehaplotype.
Evolutionary Radiations in Archipelagoes 291
resulted if L. noctis had been restricted to a single island occupied by continental bird assemblages (Schluter1988;
before its recent expansion. Burns et al. 2002).
The more common outcome of secondary expansion Divergence among allopatric populations. The average
within the Lesser Antilles is an abrupt genetic boundary distance of a species to its nearest neighbor in morpho-
between adjacent sets of island populations, within each logicalspaceisameasureofthedensityofspeciespacking
of which there is little genetic differentiation (fig. 2, case andprovidesanindicationoftheminimummorphological
IV; see below). Eight species show allopatric distribution distance consistent with coexistence. Within local assem-
ofdivergentlineageswithbreaksbetweenadjacentislands. blagesofpasserinebirdsincontinentalareas,NNDisvery
These are Saltator albicollis (Martinique-Dominica [MA- close to 0.20 log units, based on eight measurements
10
DO], 0.6%), Myiarchus oberi (MA-DO, 0.9%), Myadestes (Ricklefs and Travis 1980; Travis and Ricklefs 1983). The
genibarbis(MA-DO,1.0%),Coerebaflaveola(St.Vincent– NND within habitats on St. Lucia and St. Kitts in the
8
St. Lucia [SV-SL], 1.2%), Allenia fuscus (MA-DO, 2.4%), Lesser Antilles averaged somewhat higher (0.26 and 0.29,
Contopus latirostris/Contopus oberi (SL-MA, 3.5%), Vireo respectively),reflectingtherelativeimpoverishmentofthe
altiloquus (SV-SL, 5.2%), and Cichlherminia lherminieri avifaunaontheseislands(TravisandRicklefs1983).None-
(DO-Guadeloupe, 6.8%). In the case of V. altiloquus and theless,thevalueof0.20providesanapproximateyardstick
C. flaveola, these breaks have been verified by restriction for ecological compatibility within an assemblage of pas-
fragment length polymorphism analysis of 33 and 19 in- serine birds.
dividuals,respectively,fromSt.VincentandSt.Lucia(Lov- We calculated the divergence between allopatric pop-
etteetal.1999b).Overall,thefewcasesofsecondarysym- ulations of the same species on different islands in the
patryamongendemicLesserAntilleanbirdsstandinstark LesserAntillesbasedonmeasurementsprovidedbyRidg-
contrasttotheampleevidenceforre-expansionofranges way (1901, 1902, 1904, 1907) for the lengths of thewing,
withintheLesserAntillesleadingtoadjacentdifferentiated tail, tarsus, middle toe, and culmen (bill). For five mea-
island populations. surements, the corresponding yardstick for ecological
compatibility is NND p0.16. Comparisons were re-
5
strictedtoadjacentislands.Thus,aspeciesthatoccurson
Step 4: Morphological Divergence in Allopatry and n islands is represented by a maximumofn(cid:1)1 compar-
Compatibility in Secondary Sympatry isons, which have been averaged. Data for males and fe-
males were compared separately. In most cases, the sexes
It is a well-established principle in ecology that species differed little. The endemic thrashers (mimids, not in-
withsimilarecologicalrequirementsdonotcoexistreadily. cluding Mimus), which represent the only evolutionary
However, the degree of ecologicaldivergencerequiredfor radiation within the Lesser Antilles, were also compared
coexistenceisamatterofdebate.Moreover,thethreshold separately.
for coexistence might be smaller than the divergence ob- The average of the species means for morphological
served between species in natural assemblages because divergences (D) between allopatric populations (males
5
strong competition, while not necessarily precluding co- only) for nonmimids (0.047(cid:2)0.044 SD, range 0.021–
existence, might select for further divergence subsequent 0.074, np17) and mimids (0.056(cid:2)0.029 SD, range
to achieving secondary sympatry (Grant 1972, 1986; Ar- 0.021–0.087, np4) was less than the average NND in
thur 1982; Schluter 1996). We approach the issue of eco- passerine communities (NND ≈0.16). Divergence be-
5
logicalcompatibilitythroughananalysisofmorphological tween sympatric populations of the endemic Lesser An-
divergence of island populations in allopatry and sym- tillean mimids averaged 0.188 ((cid:2)0.049 SD, range 0.133–
patry. Presumably,evolutionaryradiationrequirestheac- 0.242, np4).
cumulation of sufficient differences between populations To investigate the rate at which morphological diver-
inallopatrythat,onsecondarysympatry,individualsfrom gence in allopatry might reach the average NND within
thedifferentpopulationsareunlikelytoreproducebutcan passerine communities with time, wecomparedmorpho-
coexist ecologically. logical distances between island populations of species in
Morphological diversification in archipelagoes. Compar- the Lesser Antilles to genetic distance. Morphological di-
isons of morphological spaces occupied by birds in the vergence (D) in allopatry was weakly related to genetic
5
Gala´pagos, Hawaiian, and Lesser Antillean archipelagoes distance in nonmimids and more strongly related to ge-
(see appendix) show that whether the source of diversity neticdistanceamongthefewmimidcomparisons(fig.3).
comes from evolutionary radiations (Gala´pagos and es- In an analysis of covariance, the slopes of these relation-
pecially Hawaii) or colonization (St. Lucia in the Lesser ships did not differ (interaction term; Fp3.7, dfp
Antilles; Travis andRicklefs 1983), birdsonarchipelagoes 1,17, Pp.070). With the interaction removed, mimids
havefilledasubstantialportionofthemorphologicalspace and nonmimids also did not differ (Fp1.1, dfp1,18,
292 The American Naturalist
Nesomimuswas5.4%,andtheaveragemorphologicaldis-
tance (D) was 0.104 (see appendix). Thus, these mock-
5
ingbirdslieclosetothemorphological-genotypicdistance
relationship observed among Lesser Antillean mimids
(predicted D p0.113).
5
In the Hawaiian honeycreepers, morphological diver-
genceamongallopatricpopulations(averageD p0.054)
5
and sympatric species (0.241) was similar to that in the
Lesser Antillean mimids (see above and appendix).How-
ever, considering that the stem age of the honeycreeper
clades is only about 6 Ma (Fleischer and McIntosh 2001;
Lovette et al. 2002) and that the average genetic distance
established between a small number of sympatric species
is 4.2% mtDNA sequence divergence, the rate of mor-
phological diversification, at least in sympatry, has been
very rapid (e.g., 0.57 units of morphological distance per
10%sequencedivergence).IntheGala´pagosGeospizinae,
Figure3:TherelationshipbetweenmorphologicalandmtDNAgenetic
divergence in Lessser Antillean passerine birds. Open circles represent divergence among sympatric species of Geospiza (D p
5
divergencebetweenadjacentislandpopulationsofthesamespecies,ex- 0.113)andCamarhynchus(0.078)issubstantiallylessthan
cludingmembersofthefamilyMimidae,whichareshownassolidcircles. the suggested yardstick for ecological compatibility
Solid diamonds represent divergence between different species of the
(0.160), but genetic distances are also small (!1.0%), in-
endemic Lesser Antillean mimids on the same island. Morphological
dicatingahigherrateofmorphologicaldiversificationthan
divergenceisbasedonfiveexternalmeasurementsfromRidgway(1901,
1902,1904,1907).Plottedvaluesareaverageswithinspeciesorsympatric in Hawaii, although morphological differences occur pri-
comparison.Errorbarsrepresentstandarddeviations.Forallopatricnon- marily on size, rather than shape, axes (see appendix).
mimids, Fp7.4, dfp1,15, Pp.016, r2p0.33, slope bp0.77(cid:2)
0.28 SE, interceptp0.042(cid:2)0.003 SE. For allopatric mimids, Fp
14.2, dfp1,2, Pp.064, r2p0.88, slope bp1.82(cid:2)0.48 SE, Discussion
interceptp0.024(cid:2)0.008 SE, tp2.8, Pp.11. For the common re-
lationship among allopatric comparisons, Fp15.5, dfp1,19, Pp Our analysis of island populations in the Lesser Antilles
.0009, R2p0.45, interceptp0.039(cid:2)0.003 SE, slopep1.01(cid:2)0.26 castsdoubtontheimportanceofevolutionarydivergence
SE. Absence of error bars for sympatric mimid comparisonsindicates (step 1), population persistence (step 2), and secondary
np1.
colonization within the archipelago (step 3) in limiting
evolutionaryradiation.Instead,itappearsthatislandpop-
Pp.32), and the common relationship indicated diver- ulations are able to achieve reproductive isolation in al-
gence in morphology in allopatry at an average rate of lopatry and ecological compatibilityinsympatry(step4).
about 0.10 distance units per 10% (∼5 Ma) sequence di- The origins of reproductive isolation. Geneticdivergence
vergence.AssuminganinterceptofDp0.04,theaverage between some allopatric island populations of LesserAn-
NND within passerine communities would be reached tillean birds is consistent with differences observed be-
at Dp0.12 (∼6 Ma), which exceeds the largest within- tweencongenericspeciesand,insomecases,relatedgenera
species differences between islandpopulationsintheLes- in both continental faunas and in the Hawaiian and Ga-
ser Antilles. la´pagosarchipelagoes.Wedonotknowwhethertheselev-
We also used ANCOVA to determine whether the re- els of genetic distance represent sufficient genetic diver-
lationship between morphological and geneticdivergence gence to produce postmating reproductive isolation
differed between allopatric and sympatric populations of amongsympatricsistertaxaoraremerelyassociatedwith
mimids. Neither the interaction term (Fp0.6, dfp the divergence of species recognition signals involved in
1,4, Pp.47) nor the difference between allopatry and prematingisolation.Eventhemostextrememitochondrial
sympatry (Fp2.5, dfp1,5, Pp.18) was significant. geneticdivergenceobservedbetweenallopatricislandpop-
When allopatric and sympatric populations were consid- ulations in the Lesser Antilles (∼7%) does not preclude
ered together, the regression of morphologicaldivergence completemixingofgenepoolsbetweenmanyhybridizing
and genetic distance had an intercept of 0.041 ((cid:2)0.023 species (Price and Bouvier 2002). Thus, behavioral/mor-
SE)andaslopeof0.134((cid:2)0.029)distanceunitsper10% phologicalchangeleadingtoprematingisolationmightbe
sequence divergence (Fp20.8, dfp1,6, P!.0039, important, or even required, for reproductive incompat-
r2p0.78). In the Gala´pagos Islands, the average genetic ibility (Alatalo et al. 1994; Grant and Grant 1996, 1998;
distance between allopatric “species” of the mockingbird Saetre et al. 1997, 2001; Veen et al. 2001). Song plasticity,
Evolutionary Radiations in Archipelagoes 293
including cultural learning, often from male parents, is morphologically (Travis and Ricklefs 1983) than in con-
prominentinsongbirds(Nowickietal.1998;Searcyetal. tinental regions, possibly leaving room for increased di-
2002), including mimids (Brenowitz and Beecher 2005), versity. Historical analysis of colonization times suggests
and might form the basis of population differentiation that the avifauna of the Lesser Antilles is well below an
sufficientforprematingincompatibility(GrantandGrant archipelago-wide equilibriumnumberofspecies(Ricklefs
1997a; Price 1998; Rundle and Schluter 1998; Simoes et and Bermingham 2001).
al. 2000). Second, as we have pointed out, contemporary diver-
Theoriginsofecologicalcompatibility.Morphologicaldis- genceinallopatryappearstobenogreaterintheHawaiian
tances between allopatric populations of Darwin’s finch and Gala´pagos passerine faunas than in the Lesser Antil-
and honeycreeper species do not exceed those between lean passerine fauna. Third, new colonists seem to enter
LesserAntilleanpasserines.Thus,competitionbetweensis- thearchipelagowithouthindrance,judgingbythefactthat
ter populations initially following secondary sympatry many recent colonists have expanded through the archi-
might not differ among these archipelagoes. However, pelago by means of multiple stepping-stone colonization
sparse occupation of ecological space in the early stages events. Although colonists from outside the archipelago
of colonization might have allowed rapid divergence in are likelytobe moredivergentfromislandresidentsthan
allopatry in response to intraspecific selectionpressureto secondarily sympatric sister populations from elsewhere
adapt to local conditions (Schluter 1988) and thus per- within the archipelago, recent colonists and endemic res-
mitted long-term coexistence. Ecological differences be- idents cannot be distinguished on the basis of the eight
tween the Lesser Antilles, Hawaii, and the New Hebrides morphologicalmeasurementsusedinthisstudy(canonical
probablyarenotimportant,asthearchipelagoeshavesim- discriminant analysis: Fp0.74, dfp8,25, Pp.66).
ilar ranges of altitude and wet-dry gradients. The drier Thus, the filling of ecomorphological space by residents
climate of the Gala´pagos Archipelago does not appear to doesnotappeartoprecludecolonizationwithinthesame
have inhibited evolutionary diversification. portion of space.
Iflimitedecologicalspacewerefilledbycolonizationin The potential role of disease organisms. An additional
theLesserAntillesandNewHebridesandtoasimilarlevel possibilitythathasnotbeenconsideredisincompatibility
by evolutionary diversification in the Gala´pagos and Ha- between native and colonizing sister populations caused
waiianarchipelagoes,thiswouldimplythattheradiations by shared pathogens—apparent competition (Holt 1977;
of Gala´pagos and Hawaiian birds slowed over time. In- Holt and Lawton 1994; Bonsall and Hassell 1997; Chane-
sufficient phylogenetic evidence is available to test this tonandBonsall2000;Tompkinsetal.2000,2002;Morris
idea. It might be significant that the oldest extantlineage etal.2004).Colonistsbringwiththempathogenstowhich
in the Lesser Antilles (14.3%; Hunt et al. 2001; Ricklefs theyhaveevolvedeffectiveresistance,andthesepathogens
and Bermingham 2001), which is comparable in age to might depress potential local host populations. The ex-
the colonization of Hawaii by ancestors of the drepanids tinctionandnearextinctionofmanynativeHawaiianbirds
andtheHawaiianthrush(13%–18%;Lovetteetal.2002), by introduced malaria andpoxvirus providesamodelfor
was the ancestor of the present-day endemic thrashers. this mechanism (Van Riper et al. 1986; Jarvi et al. 2001).
Thesubsequentfillingofecologicalspacemightalsohave The apicomplexan blood parasites Plasmodium and Hae-
reduced the rate of establishment of new colonists from moproteus exhibit significant host species#island inter-
the continent; however, estimated colonization times for actionsinprevalenceintheLesserAntilles(Apaniusetal.
passerines in the Lesser Antilles provide no indication of 2000; Fallon et al. 2003), indicating island-specific host-
slowing (Ricklefs and Bermingham 2001). Unfortunately, pathogen relationships that could result from coevolu-
we have no information on the relative ages of New He- tionary interactions in genetically isolated island popula-
brideanbirds.Thelowlevelofendemism,evencompared tions. If parasites evolved locally to host populations on
withlevelsintheLesserAntilles,suggestsrecentderivation oneisland,hostsisterpopulationsonotherislandswould
of the avifauna. notbeselectedtoacquireresistance.Inthisway,secondary
Although competitive exclusion owing to lack of dif- sympatry could be prevented by dangerous pathogensei-
ferentiationmightexplainecologicalincompatibilityofsis- ther carried to or encountered in a novel island setting.
ter populations on islands, several considerations weigh This mechanism of incompatibility between secondarily
againstthis.First,mostislandsharborrelativelyfewspecies sympatric sister populations might be absent from infre-
of birds compared to continental areas with similar en- quently colonized archipelagoes, such as Hawaii and Ga-
vironments.Thus,atpresent,habitatsintheLesserAntilles la´pagos. Disease organisms might be poorly represented
arerelativelyless“saturated”ecologically(RicklefsandCox in such remote locations owing to the small number of
1978; Cox and Ricklefs 1977; Terborgh et al. 1978; Ter- colonizinghosts(speciesandindividuals),lackofsuitable
borgh and Faaborg 1980; Travis and Ricklefs 1983) and vectors, and stochastic loss of pathogens from host pop-
294 The American Naturalist
ulations on isolated islands (e.g., Van Riper et al. 1986; and Darwin’s finches originated from groups exhibiting
Font and Tate 1994; Krebs et al. 1998). high morphological diversity in beak dimensions among
continentalandWestIndianspecies,indicatingapropen-
sityforevolutionaryradiation.Evolutionaryradiationalso
Conclusions
mightbeamatterofchance(Ricklefs2003).Ineithercase,
Whatdocomparisonsbetweenarchipelagoestellusabout thesmallnumberoflineagesthathavediversifiedprovides
evolutionarydiversification?First,inmanyspecies,move- little statistical power to assess causative factors through
ment of individuals between islands is too infrequent to comparative analysis. Nonetheless, many avenues for in-
preventdiversificationinallopatry.EvenintheLesserAn- vestigating evolutionary radiation remain. These include
tilles, where new colonists rapidly islandhopthroughthe phylogeneticandecomorphologicalcharacterizationofra-
archipelago, most of the widespread taxa and all of the diations, particularly in comparison to lineages that have
older restricted taxa exhibit fixed genetic differences be- not diversified (Schluter 1988; Losos 1995; Losos et al.
tween some island populations. Thus, gene flow between 1998;KornfeldandSmith2000;Burnsetal.2002;Lovette
islands is often too low to prevent differentiation, even et al. 2002), studies of the abundance and host distribu-
withrespecttoapparently“neutral”geneticvariation.Sec- tions of pathogens in remote and near groups of islands
ond,someindividualislandpopulationsintheLesserAn- (Ricklefs and Fallon 2002; Fallon et al. 2003), and exper-
tilles are as old as many secondarily sympatric species of imental studies of premating isolating mechanisms be-
honeycreepers in the Hawaiian archipelago or the entire tween allopatric populations (Grant and Grant 1997b;
radiation of Darwin’s finches in the Gala´pagos Archipel- Coyne and Orr 2004). Certainly, evolutionary radiations
ago. Thus, the persistence of island populations long on islands remain one of the most important systemsfor
enough to establish reproductive isolation—primarily by understanding the process of speciation.
prezygoticmechanisms—inanallopatricmodelofspecies
formation shouldnot hindersecondarysympatry,atleast Acknowledgments
not in the Lesser Antilles. Third, secondary colonization
Our research on birds in the West Indies has been sup-
ofislandsoccursrelativelyfrequently,asshownbyrecently
portedgenerouslybytheSmithsonianInstitution,theNa-
expanded distributions of endemic Lesser Antillean pas-
tionalGeographicSociety,andtheNationalScienceFoun-
serinebirds(RicklefsandBermingham1999,2001).Thus,
dation, as wellas by the laboratoryandfieldassistanceof
noneofthesestepsinspeciesformationthroughallopatric
M. Gonzalez, I. Lovette, and G. Seutin, among others.
divergencefollowedbysecondarycolonizationappearsto
Fieldwork would not have been possible withouttheper-
limit evolutionary diversification.
mission and cooperation of many government agencies
Although similar data are lacking for other archipel-
and individuals throughout the West Indies. We thank
agoes, the general absence in the Lesser Antilles of pop-
severalanonymousreviewersforcommentsonthemanu-
ulationswithmixeddivergentlineagesindicatescontem-
script.
porary as well as historical impediments to secondary
sympatry.Itmaybesignificantthattwoofthethreecases
indicatingcoexistingdivergentmtDNAlineagesoccurred Literature Cited
among the endemic Lesser Antillean thrashers (Margar-
Alatalo,R.V.,L.Gustafsson,andA.Lundberg.1994.Malecoloration
opsfuscatus,Cinclocerthiaruficauda),whichbelongtothe and species recognition in sympatric flycatchers. Proceedingsof
only radiation of passerine birds in the archipelago.The theRoyalSocietyB:BiologicalSciences256:113–118.
paucityofmixingandintrogressionfurthersuggeststhat Allmon,W.D.1992.Acausalanalysisofstagesinallopatricspeci-
the problem with compatibility is not primarily ecolog- ation.OxfordSurveysinEvolutionaryBiology8:219–257.
Amadon,D.1950.TheHawaiianhoneycreepers(Aves,Drepaniidae).
ical, because this presumably would not prevent mixing
BulletinoftheAmericanMuseumofNaturalHistory95:151–262.
of reproductively compatible nativeandcolonizingpop-
AmericanOrnithologists’Union.1998.Check-listofNorthAmerican
ulations.Ifcoexistenceweremademoredifficultthrough
birds.AmericanOrnithologists’Union,Washington,DC.
apparent competition mediated by pathogens, then eco- Apanius, V., N. Yorinks, E. Bermingham, and R. E. Ricklefs. 2000.
logicalcompatibilitymightbelessofaprobleminremote Island and taxon effects in parasitism and resistance of Lesser
islands, which have fewer suitable disease vectors and Antilleanbirds.Ecology81:1959–1969.
fewer lineages of disease organisms. Arthur,W.1982.Theevolutionaryconsequencesofinterspecificcom-
petition.AdvancesinEcologicalResearch12:127–187.
Whydosomelineagesdiversifyandothersdonot?Par-
Avise,J.C.1994.Molecularmarkers,naturalhistory,andevolution.
ticular attributes of some lineages might promote diver-
Chapman&Hall,NewYork.
sification(HeardandHauser1995;Barracloughetal.1998;
Barraclough, T. G., S. Nee, and P. H. Harvey. 1998. Sister group
RicklefsandRenner2000).Lovetteetal.(2002)andBurns analysis in identifying correlates of diversification. Evolutionary
et al. (2002) suggested that the Hawaiian honeycreepers Ecology12:751–754.