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The origins of tropical marinebiodiversityBrian W. Bowen1, Luiz A. Rocha2, Robert J. Toonen1, Stephen A. Karl1, andthe ToBo Laboratory*

1 Hawaii Institute of Marine Biology, School of Ocean and Earth Science and Technology, University of Hawaii, P.O. Box 1346,

Kaneohe, HI 96744, USA2 California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA 94118, USA

Review

Glossary

Biodiversity feedback: biogeographic model with biodiversity hotspots acting

as both Centers of Speciation and Centers of Accumulation and/or Overlap.

Biodiversity hotspot: region with especially high levels of biodiversity as

measured by species numbers and levels of endemism. Conservation of

biodiversity hotspots should aim at preserving not just species diversity but

also the mechanisms underlying biodiversity production.

Center of Accumulation model: this model suggests that the high number of

species in the Coral Triangle results from speciation in peripheral locations with

subsequent dispersal of novel taxa into the Coral Triangle. The long history of the

Pacific archipelagos, some of which date to the Cretaceous, the possibility of

isolation in these peripheral habitats, and current and wind patterns that favor

dispersal towards the Coral Triangle have been suggested as a mechanism.

Center of Overlap model: this model suggests that the high species diversity in

the Coral Triangle is in part due to overlap of distinct faunas from the Pacific

and Indian Oceans. The hypothesis is based on the premise that the isolating

mechanism is the Indo-Pacific Barrier, which separates the Pacific and Indian

Oceans during low sea-level stands, with the faunas of these oceans diverging

during periods of isolation.

Center of Speciation model: also known as the Center of Origin, this

Recent phylogeographic studies have overturned threeparadigms for the origins of marine biodiversity.(i) Physical (allopatric) isolation is not the sole avenuefor marine speciation: many species diverge along eco-logical boundaries. (ii) Peripheral habitats such as oce-anic archipelagos are not evolutionary graveyards: theseregions can export biodiversity. (iii) Speciation in marineand terrestrial ecosystems follow similar processes butare not the same: opportunities for allopatric isolationare fewer in the oceans, leaving greater opportunity forspeciation along ecological boundaries. Biodiversity hot-spots such as the Caribbean Sea and the Indo-PacificCoral Triangle produce and export species, but can alsoaccumulate biodiversity produced in peripheral habitats.Both hotspots and peripheral ecosystems benefit fromthis exchange in a process dubbed biodiversity feedback.

The enigma of speciation in the seaOver half a century ago Ernst Mayr posed the question ofwhether speciation is fundamentally different in the sea[1]. On the basis of studies of sea urchins, he concluded thatthe process was the same in marine and terrestrial faunas,but this controversy flared across ensuing decades. Much ofthe debate centered on the relative importance of geneticisolation versus dispersal in a scientific era in whichphysical (allopatric) barriers were regarded as the prima-ry, if not exclusive, starting point for speciation [2,3]. Thereare few obvious physical barriers in the ocean, and dis-persal is extensive in this transglobal aquatic medium; twofactors that should reduce opportunities for allopatricspeciation [4]. Yet tropical reefs host biodiversity thatrivals that in rainforests. Coral reefs cover less than0.1% of the ocean floor [5], but their fish communitiesinclude approximately one-third of the recognized marine

0169-5347/$ – see front matter

� 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2013.01.018

Corresponding author: Bowen, B.W. (bbowen@hawaii.edu).* Members of the ToBo (Toonen/Bowen) Laboratory who contributed to this paper

are Matthew T. Craig (Department of Marine Science and Environmental Studies,University of San Diego, San Diego, CA 92110, USA), Joseph D. DiBattista (Red SeaResearch Center, King Abdullah University of Science and Technology, Thuwal, SaudiArabia), Jeff A. Eble (Center for Environmental Diagnostics and Bioremediation,University of West Florida, Pensacola, FL 32514 USA), Michelle R. Gaither2, DerekSkillings1, and Chris J. Bird (Department of Life Sciences, Texas A&M UniversityCorpus Christi, 6300 Ocean Drive, Corpus Christi, TX, 78412 USA).Keywords: biodiversity feedback; biogeography; center of accumulation; center ofspeciation; ecological opportunity; marine speciation; phylogeography.

species. In these circumstances it is impossible to reconcilethe prevailing beliefs about speciation by allopatric isola-tion with the plethora of closely related species livingtogether in the sea.

If cessation of gene flow by geographic isolation is thekey to terrestrial speciation, then intuitively the processesleading to speciation should be different between marineand terrestrial habitats. Most marine organisms movelittle as juveniles and adults, so connectivity must bethrough pelagic (oceanic) stages such as larvae, and insome cases this dispersal can be extensive. Whereas somereef fauna show self-recruitment over small geographicranges [6], the majority have oceanic dispersing larvaethat can contribute substantially to connectivity amongregions [7]. Marine biotas show a broad range of dispersalcapabilities [8], from crawl-away larvae to pelagic dispers-al that is at least an order of magnitude greater than the

biogeographic model suggests that tropical biodiversity hotspots including

the Coral Triangle are exporters of species, possibly driven by the fracture of

populations that result from geologic complexity and habitat heterogeneity

coupled with intense competition.

Coral Triangle: epicenter of marine biodiversity, with over 2700 species of shore

fishes and 600 species of corals, that extends from the Philippines, eastern

Indonesia and New Guiana southeast to the Solomon Islands (see Figure 1 in

main text).

Evolutionary graveyard: the premise that depauperate peripheral habitats act

solely as sinks of biodiversity and contribute little to overall species richness.

Gametic recognition proteins (GRP): cell surface proteins that mediate the

interactions between gamete cells with incompatibility, resulting in unsuccess-

ful fertilization. Rapid evolution of GRPs is thought to be an important driver of

speciation in some taxa.

Trends in Ecology & Evolution xx (2012) 1–8 1

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capabilities of pollen-dispersing terrestrial biotas [9]. Forexample, moray eels (family Muraenidae) show high pop-ulation genetic connectivity across two-thirds of the planet,from Africa to Central America [10], unicornfishes (Nasospp.) show no genetic isolation across the Indian andPacific Oceans [11], and even the diminutive pygmy angel-fishes (genus Centropyge) show high genetic connectivityacross thousands of kilometers [12]. To the extent thatdispersal and gene flow influence speciation, the processcannot be the same on land and sea, or must work on vastlydifferent scales. Here we review recent work indicatingthat (i) speciation in the sea can proceed without absolutebarriers to gene flow, (ii) peripheral habitats such as theHawaiian Archipelago and Red Sea can produce and exportnew species, and (iii) exchange of biota among extremelycompetitive hotspots and depauperate peripheral areas isa process that enhances species numbers and ecosystemresilience in both areas, which we term the biodiversityfeedback model (see Glossary) [13]. This synthesis arisesprimarily from efforts to resolve the origins of marinebiodiversity hotspots, including three apparently overlap-ping hypotheses reviewed in the next section.

Biodiversity hotspotsJohn Briggs has been the primary advocate of marinecenters of speciation, among which the Coral Triangle inthe Indo-Pacific (also known as Indo-Australian Archipel-ago or Indo-Malayan Triangle, the area betweenIndonesia, New Guinea, and the Philippines in Figure 1)and the Caribbean Sea in the Atlantic are cradles for newspecies that radiate out and replace older species [14].Under this model, intense competition in highly diversehabitats yields new species with greater fitness than theirpredecessors. A combination of physical and ecologicalpartitioning is probably the most effective means to estab-lish new species. Therefore, isolated populations withinthe Coral Triangle might be the precursors of speciationand subsequent radiations [15–17].

The distribution of reef fishes is consistent with thismodel [18] and it is apparent that much of the biodiversityin peripheral archipelagos has arrived from the central

30° 60 ° 120° 1

Figure 1. Biogeographic provinces of the tropical West Atlantic and Indo-Pacific (indic

flows out from the Coral Triangle (light blue in central Indo-Pacific) to peripheral habitats

can colonize the depauperate coastline of Brazil. Species diverging in these peripheral

2

Indo-Pacific [19]. Recent evidence indicates that two reef-associated sharks (Sphyrna lewini and Triaenodon obesus)radiated from the central Indo-Pacific to attain broad orglobal distributions [20,21]. Two new reviews provide con-cordant assessments for the Coral Triangle hotspot, in-cluding a long history of species accumulation beginning inthe Miocene [20–12 million years ago (mya)] and subse-quent export of biodiversity in the Pliocene, Pleistocene,and Holocene (7 mya to the present) [22,23].

A corollary of the Center of Speciation hypothesis is thatareas peripheral to biodiversity hotspots are evolutionarygraveyards, where colonizers arrive and evolve into en-demic species, but never radiate beyond their new home.This is supported by studies of the isolated Hawaiianfauna, including fish, corals, and other invertebrates[24–26]. Recent studies have prompted a reappraisal ofthis corollary, which we examine below.

A primary alternative to the Center of Speciation hy-pothesis is a Center of Accumulation, in which new speciesarise in peripheral habitats such as oceanic archipelagosand accumulate in the center of the range because ofprevailing currents [27,28]. Support for this model comesfrom several phylogeographic studies (see below). Buddand Pandolfi note that morphological novelty is highest atthe edge of coral species distributions, consistent with theCenter of Accumulation model [29].

A related model is the Center of Overlap, in whichisolated faunas of the Indian and Pacific Oceans are codis-tributed in the area of overlap, including the Coral Trian-gle. The biogeographic case for Center of Overlap includesthe many sister species with Pacific and Indian Oceandistributions that overlap at the boundary of these oceans[30]. Gaither et al. observed two mtDNA lineages in thegrouper Cephalopholis argus corresponding to Indian andPacific Oceans but overlapping in the boundary regionsbetween these oceans (including the Coral Triangle;Figure 1) [31].

Overall, there is substantial evidence in support of allthree processes according to recent phylogeographic stud-ies of tropical marine fauna [13,32,33]. Whereas the Centerof Speciation model involves speciation without complete

80° 120°

30°

30°

0°

TRENDS in Ecology & Evolution

ated in blue) [23,93]. The Biodiversity Feedback model indicates that biodiversity

in Hawaii, the East Pacific, Red Sea, and elsewhere. In the Atlantic, Caribbean fauna

habitats can subsequently radiate back out to enhance overall biodiversity [22,23].

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geographic isolation (allopatry), the other two models in-clude some level of allopatric isolation, which raises thequestion as to whether isolation plays a leading role inmarine speciation.

Speciation without geographic barriersSpeciation via allopatry, as proposed by Dobzhansky [34]and Mayr [2], continues to be the dominant paradigm inevolutionary biology [35]. By contrast, molecular phylog-enies of marine organisms provide many examples ofsister taxa with distributions that are adjacent (parapa-tric), overlapping, or even identical (sympatric). In agrowing body of literature, non-allopatric speciation isinferred from phylogenetic data combined with distribu-tion data and ecological partitions (Box 1). Examples of

Box 1. Cases of non-allopatric speciation

Caribbean and East Pacific reef fish,

collectively known as grunts (genus

Haemulon), show numerous exam-

ples of sympatric sister species [50].

Vocalization may be key to mate

recognition in the darkness as these

fishes spawn at night. It is suspected

that sexual selection on the basis of

vocal cues promotes reproductive

isolation among sister species.

Photo: L.A. Rocha.

Sister species of brown algae (genus

Fucus) segregate along a steep inter-

tidal gradient despite ongoing hybridi-

zation. Common garden experiments

show that physiological resistance to

desiccation in each species is com-

mensurate with intertidal exposure

time [94]. Photo: K.R. Nicastro.

Caribbean wrasses (Halichoeres

spp.) reveal intraspecific genetic

partitions between adjacent and

ecologically distinct habitats, but

high genetic connectivity between

similar habitats separated by thou-

sands of kilometers [95]. Photo: L.A.

Rocha.

The Caribbean sponge Chondrilla

caribensis has two ecotypes, one

proposed ancestral ecotype adapted

to reef habitats and another specia-

lized for mangrove habitats. These

ecotypes, long described as a single

species, have been distinguished on

the basis of morphology and genetics

[96]. Photo: K. Ruetzler.

The Caribbean basslet Gramma

dejongi has a restricted geographic

range completely encompassed by

the widespread sister species G.

loreto. In describing this species,

Victor and Randall note that G.

dejongi has a narrower depth range

than G. loreto [97]. Photo: B. Victor.

sympatric sister species have been documented in adiversity of taxa including East Pacific fishes [36], NorthAtlantic snails [37], and Caribbean sponges [38]. Amongthe most intriguing examples are sympatric species thatseem to maintain separate identities despite ongoinggene flow, including Pacific pygmy angelfishes (Centro-pyge flavissima complex) [12], Caribbean hamlets (genusHypoplectrus) [39], and sea stars (Linckia multiflora andLinckia laevigata) [40] (Figure 2). These may representthe earliest stages of speciation.

In addition to overlapping sister species, numerousexamples have emerged of sister species with adjacentdistributions. Caribbean gobies (genus Elacatinus) haveseveral color morphs with parapatric distributions, forwhich coloration differences might facilitate assortative

The brooding coral Seriatopora

histrix shows genetic partitions be-

tween adjacent habitat types on the

Great Barrier Reef [98], prompting

the authors to conclude that ‘adap-

tation to the local environment has

caused ecological divergence of

distinct genetic groups within S.

hystrix.’ Photo: J. Sprung.

West Pacific reef fishes include

several examples of sympatric sister

species characterized by habitat

shifts, including gobies (Gobiodon

spp.) [99]. In this case, sympatric

speciation has been accompanied

by a host shift between Acropora

corals. Photo: P.L. Munday.

Hawaiian limpets (Cellana spp.)

comprise three sympatric sister spe-

cies that partition along ecological

lines into upper, middle, and lower

intertidal zones. Habitat partitioning

is thought to be caused by desicca-

tion, thermal tolerance, and/or pre-

dation avoidance mechanisms, and

reproductive isolation may be ac-

complished by the timing of ga-

metic release [91]. Photo: C.L. Bird.

Nudibranchs (genus Phestilla) form a

close bond with their scleractinian coral

host, feeding, reproducing, and requiring

host-specific chemical cues for settle-

ment. Phylogenetic analyses revealed

several incidences of host-shifting ac-

companied by speciation [89]. Photo: R.

Williams.

3

(a) (b)

(c) (d)

(e) (f)

TRENDS in Ecology & Evolution

Figure 2. Sister species with overlapping distributions that maintain striking color differences despite apparent gene flow: (a) Hypoplectrus puella and (b) Hypoplectrus

gemma in the Caribbean Sea [39]; (c) Centropyge vrolikii and (d) Centropyge flavissima in the West Pacific [12]; and (e) Linckia multiflora and (f) Linckia laevigata in the West

Pacific [40]. Photos: L.A. Rocha and G. Paulay.

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mating at range boundaries [41]. The Dascyllus trimacu-latus species complex of four closely related Pacific damsel-fishes has parapatric distributions [42]. Particularlyinteresting cases of parapatry include highly mobile ma-rine vertebrates with ecotypes that segregate into adjacent(often inshore and offshore) morphotypes, a phenomenonobserved in marine mammals [43,44], sharks [45], andmanta rays [46]. These species are all capable of vastdispersal and yet retain genetic partitions along ecologicalboundaries.

These and many other examples have promptedresearchers to resurrect ecological factors as primary dri-vers in marine speciation [47]. This Darwinian view ofselection driving speciation is a marked departure fromthe era of vicariant biogeography, when speciation wasdefined in terms of geography and physical isolation [3].Clearly, a single model of speciation via allopatric isolation

4

is insufficient to describe the diversity of species in the sea.The combination of hard, soft, or intermittent barriers (suchas oceanic currents, water masses, expanses of deep ocean,or land masses exposed during glaciation) and ecologicaldifferences between adjacent areas represents a middleground between speciation in sympatric or allopatric isola-tion, a very fertile circumstance for speciation in the sea[4,48].

A counterargument to these cases of apparent sympat-ric speciation is based on allopatric speciation with subse-quent range expansion and secondary contact. Under thisscenario, speciation occurs in isolation but then speciesranges expand to overlap [49]. This explanation of histori-cal changes in geographic distribution is very difficult todisprove, and is almost certainly correct in some cases.Isolation followed by secondary contact can explain diver-sification within the Coral Triangle for less dispersive

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species (e.g., the clownfish Amphiprion ocellaris) [16]. It isharder, however, to fit this hypothesis to recently derivedspecies (such as the grunts, Haemulon spp.) in which manysister species have entirely overlapping distributions [50].

Several research groups have concluded that sympatric(or parapatric) speciation is faster than the allopatric alter-native [35,51], averaging approximately 200 000 yearsversus 2.7 million years in Drosophila, presumably be-cause selection can establish a reproductive barrier morerapidly than random genetic drift due to physical isolation[52,53]. Rapid evolution of gametic recognition proteins(bindins) can facilitate the final stages of reproductiveisolation [54]. Examples of rapid speciation include ma-rine snails [55], seastars [56], and marine fishes [57].Recent modeling studies indicate that the more rapidspeciation in sympatry or parapatry is likely driven bya combination of sexual selection (mate recognition andassortative mating) combined with adaptive naturalselection for alternative habitats [58].

Peripheral habitats can export new speciesThe Center of Speciation versus Center of Accumulationand/or Overlap hypotheses cast oceanic islands in opposingroles. In the Center of Speciation model, islands are evolu-tionary dead ends, whereas in the Center of Accumulationand/or Overlap, islands are engines of biodiversity produc-tion. Recent studies have evaluated these alternatives.Although some ocean island endemics appear to be relicpopulations of previously widespread species [19], manyhave become established recently (neo-endemic; e.g., Tha-lassoma spp.) [32], with their presence demonstratingevolutionary innovation around oceanic islands.

Accumulated evidence indicates that areas peripheralto biodiversity hotspots are exporting genetic and biolog-ical diversity [59]. The ember parrotfish (Scarus rubro-violaceus) occurs throughout the Indo-Pacific, butpopulation genetic data indicate that larval export fromHawaii is an order of magnitude greater than import [60],and this ratio is even higher for the deepwater crimsonjobfish Pristipomoides filamentosus [61] and the lollyfishsea cucumber Holothuria atra [62]. The bullethead par-rotfish (Chlorurus sordidus) has three distinct mtDNAlineages corresponding to the Indian Ocean, the WestPacific, and Hawaii. However, fish collected in the North-ern Marianas Islands (westward and down-current fromHawaii) have the Hawaiian lineage, indicating a period ofextended Hawaiian isolation followed by more recentlarval export [63]. Migration estimates for the Indo-Pacific yellow tang (Zebrasoma flavescens) are similarto those for the ember parrotfish, with a prevailing pat-tern of larval export from Hawaii [64]. Moreover, yellowtang ecology, historical demography, and phylogeneticspoint to a Hawaiian origin for this widely distributed reeffish. Hence, Hawaii is both a source and recipient of Indo-Pacific marine diversity.

The Red Sea can also export unique genetic lineages toadjacent regions. Despite a volatile geological history char-acterized by intermittent isolation and multiple salinitycrises, mtDNA distributions of widespread reef fish speciesindicate that some species originate in the Red Sea withsubsequent export to the Indian Ocean [65].

Isolated archipelagos and peripheral seas are not theonly sources conveying species into areas of higher biodi-versity. The continental coastlines of the Indo-Pacific andAtlantic can also provide evolutionary novelties. The par-rotfish genus Scarus includes two basal lineages (Scaruszufar and Scarus collana) endemic to the coastlines of thenorthern Indian Ocean and Red Sea [66]. The continentalreefs of the tropical eastern Pacific have contributed atleast 23 species to the Central Pacific [67]. Much of the reeffauna of the eastern tropical Pacific are derived from thecentral Indo-Pacific, involving migration events across thevast open ocean between the Central and East Pacific(Figure 1). However, phylogeographic studies indicate re-cent or ongoing connections in both directions [68]. In thetropical Atlantic, the Caribbean is recognized as a biodi-versity hotspot with approximately 814 reef fishes, and theBrazilian coastline is a depauperate outpost of this faunawith approximately 471 species [69]. Most of the Brazilianfauna is derived from the Caribbean, but Brazil alsoexports both genetic diversity and fish species back intothe Caribbean [13].

These studies demonstrate that isolated islands, mar-ginal seas, and peripheral coastlines are not evolutionarygraveyards for marine fauna. We anticipate that with moreinvestigations, the number of examples of biodiversityexport from peripheral areas will grow. Clearly, biodiver-sity production in tropical seas does not fall easily into amodel of a Center of Speciation, Accumulation, or Overlap,but requires a more inclusive model that incorporates all ofthe observed patterns.

Biodiversity feedback: a new paradigmIn recent years a number of phylogeographic studies havetested whether the youngest lineages or species are inbiodiversity hotspots (favoring Center of Speciation) orin peripheral habitats (favoring Center of Accumulationand/or Overlap). The results have been mixed. Barber et al.support a Center of Speciation on the basis of the geneticarchitecture of mantis shrimp (Stomatopods) [15], andsimilar patterns have been reported for mangroves(Rhizophoraceae) [70] and turban snails (Gastropoda)[71]. Teske et al. support the Center of Accumulation modelon the basis of seahorse (Hippocampus spp.) phylogenetics[72]. In a survey of eight fishes, four corals, and onemollusk, Halas and Winterbottom observed evidence forboth hypotheses [73]. Phylogeographic patterns in wrasses(Halichoeres spp. and Thalassoma spp.) also support bothmodels [32,74]. These studies laid the foundations for thecurrent synthesis, with the recognition that these modelsare not mutually exclusive. The new biodiversity feedbackmodel [13] incorporates elements of all three previousmodels (Box 2).

There is no question that allopatric speciation occurs inthe sea, and many examples have emerged from phylogeo-graphic studies [75]. It is also clear that rare dispersalevents to oceanic archipelagos, followed by isolation andspeciation, are an important evolutionary process respon-sible for the high level of endemism in remote archipelagos[76,77]. The paradigm shift here is that these marinespecies can sometimes radiate further and escape theevolutionary dead end of peripheral isolation. In Hawaii,

5

Box 2. The false dichotomy between competing

hypotheses in ecology and evolution

The scientific method mandates testing of alternate hypotheses, with

predictions of each hypothesis evaluated using empirical data. In

many fields of science, testing of alternative hypotheses is a robust

approach. For instance, the physical particles that comprise atoms

have a positive, negative, or neutral charge, and none of these labels

can apply simultaneously. In biology, a more nuanced approach is

required, because multiple explanations are needed to explain

complex biological patterns. For example, hypotheses for the

navigation of migratory birds involve celestial clues (stars and sun)

or sensing of the geomagnetic field of the earth, when in fact each is

correct for individual species and some species use both [100].

Likewise, the Center of Speciation, Center of Accumulation, and

Center of Overlap models are not mutually exclusive, but instead are

operating in concert. In a recent review of paleontological data and

species histories, Cowman and Bellwood conclude that the Coral

Triangle had a long history of biodiversity accumulation stretching

back to the Eocene, with subsequent diversification and contempor-

ary export of species [22]. Briggs and Bowen reach a similar

conclusion, that the Coral Triangle was a museum of biodiversity

(accumulation) before it could be a cradle of speciation (export) [23]. A

second dichotomy explored here is the competing hypotheses of

speciation with or without geographic isolation. The emerging

consensus is that both are important, and biodiversity may be highest

when they work in concert, particularly for emerging species with

adjacent (parapatric) ranges with alternative ecological regimes [4].

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the yellow tang [64], lollyfish [62], bullethead parrotfish[63], and ember parrotfish [60] have exported genetic andbiological diversity, and export of biodiversity to the CoralTriangle has been shown for the lemon damselfish (Poma-centrus moluccensis) [78]. Rather than being an evolution-ary graveyard, peripheral habitats can export biodiversity.

The ecological component of speciationAlthough isolation can explain much of marine biodiversi-ty, there is growing recognition that speciation in the seacan also occur in the presence of gene flow. The consensus isthat this occurs when divergent selection overwhelms thehomogenizing effect of gene flow [79,80].

New species can arise through intense competition inbiodiversity hotspots, and these may constitute the major-ity of novel evolutionary lineages. However, new speciesare also evolving under conditions of ecological release inthe depauperate archipelagos that surround biodiversityhotspots. In the Coral Triangle, a carnivorous grouper(family Epinephelidae) might overlap with over 100 othergrouper species, in particular 15 members of the wide-spread genus Cephalopholis with similar ecology and diet[81]. Under such conditions, there is a premium on habitatpartitioning and specialization that leads to rapid specia-tion, with subsequent radiation of the fitter species intonew areas. In the peripheral archipelago of Hawaii, anintroduced grouper (C. argus) has to contend with no othermembers of the genus and only one other member of thetaxonomic family [82], so that ecological release hasallowed expansion of niche breadth [83]. This pattern isconsistent with the ecological opportunity hypothesis pro-posed by Simpson [84] and recently supported by empiricalstudies [85,86]. The intense competition in the center, inconjunction with ecological release at the periphery,results in biodiversity feedback that produces more speciesthan either process could alone.

6

Marine versus terrestrial speciationIt remains to be seen whether biodiversity feedback isoperating in terrestrial hotspots, but our focus remains onthe tropical reef ecosystems that are the heart of marinebiodiversity. In a departure from our illustrious predeces-sors, new research indicates that speciation has a differentblend of processes in the sea. As noted by Dawson andHamner [87], there is no hard dichotomy between speciationmechanisms in marine and terrestrial spheres; diversifica-tion is proceeding along both geographic and ecologicalpartitions. However, the greater dispersal ability of mostmarine organisms reduces the prevalence of the former andtips the balance towards the latter. This contrast is clearlyillustrated in the natural history of the Hawaiian Islands.Above the waterline, hundreds of terrestrial species haveradiated from single rare colonization events. Examplesrange from flowering plants to insects to birds, and thefootprints of allopatric speciation are strong [88]. Belowthe waterline, however, allopatric divergence is apparentin low-dispersal species, but radiations within the archipel-ago have a stronger ecological component [89–91]. Anotherimportant distinction is that Hawaii exports marine biodi-versity, whereas exports of terrestrial diversity are virtuallyunknown. Hence, it is apparent that the origins and main-tenance of biodiversity are starkly different in the sea, as isthe prevalence of various mechanisms of speciation.

Concluding remarksTwo decades of phylogeographic research indicate thatboth allopatric and sympatric speciation is occurring inmarine ecosystems, with the combination of ecologicaldivergence and partial isolation (parapatry) perhaps offer-ing the richest opportunities for diversification. Marinebiodiversity hotspots are wellsprings that export species,but isolated archipelagos, marginal seas, and depauperatecoastlines also contribute to overall biodiversity. Further-more, the interaction between hotspots and peripheralhabitats can boost biodiversity in both. The Indo-Pacifichotspot with the greatest diversity has a halo of archipela-gos in both the Indian Ocean and (especially) the PacificOcean. The Caribbean hotspot has no halo, but has dem-onstrated feedback with depauperate Brazilian reefs [13].Under this biodiversity feedback model, the islands thatsurround the central Indo-Pacific Coral Triangle are es-sential to the processes that support the highest marinebiodiversity on the planet.

Although phylogeographic and phylogenetic studies setthe stage for this paradigm shift, the field is entering a vastnew stage of exploration. It is now possible to read entiregenomes and divide genomes into arrays of neutral loci andregions under selection [58]. In abundant cases of sus-pected speciation by natural selection in sympatry (versusallopatry and secondary contact), genomics will revealwhich loci are under selection and whether these areresponsible for evolutionary divergences that are thefoundation of biodiversity. New coalescent modelingapproaches hold promise for revealing the timing of thecessation of gene flow and the relative roles of drift andselection responsible for evolutionary divergences [92]. It iscertain that paradigms will fall, new ones will rise, andscience will take a giant step towards the resolution of

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Darwin’s mystery. Furthermore, it is apparent that ifhuman minds can conjure a plausible speciation mecha-nism, then nature can probably provide an example, andperhaps more as yet undreamed.

AcknowledgmentsThis synthesis greatly benefited from discussions with J.C. Briggs, F.W.Allendorf, K.R. Andrews, J.C. Avise, P.H. Barber, D.R. Bellwood, G.Bernardi, J.H. Choat, J. Copus, I. Fernandez-Silva, Z. Forsman, W.S.Grant, P. Jokiel, R. Kinzie, H. Lessios, G. Paulay, R. Pyle, J.E. Randall, C.Rocha, J. Roughgarden, and Z. Szabo. We thank the director and staff ofthe Hawaii Institute of Marine Biology, R. Kosaki, D. Pence, andmembers of the ToBo Laboratory for logistic assistance. For photographswe thank P.L. Munday, R. Myers, K.R. Nicastro, J.R. Pawlik, G. Paulay,J.E. Randall, K. Ruetzler, J. Sprung, B. Victor, and R. Williams. We alsothank Editor P. Craze, H. Choat, and an anonymous reviewer for valuablesuggestions and guidance. Studies of Indo-Pacific reef fauna by the ToBoLaboratory were supported by the National Science Foundation (OCE-0453167 and OCE- 0929031 to B.W.B., OCE-0623678 to R.J.T.), theUniversity of Hawaii Sea Grant College Program, the Seaver Institute (toB.W.B), the National Geographic Society (to M.T.C. and J.D.D.), theNOAA Office of National Marine Sanctuaries (to R.J.T.), and theCalifornia Academy of Sciences (to L.A.R.). This is HIMB publication1544 and SOEST publication 8878.

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