quaternary coral reef refugia preserved fish diversity

5
DOI: 10.1126/science.1249853 , 1016 (2014); 344 Science et al. Loïc Pellissier Quaternary coral reef refugia preserved fish diversity This copy is for your personal, non-commercial use only. clicking here. colleagues, clients, or customers by , you can order high-quality copies for your If you wish to distribute this article to others here. following the guidelines can be obtained by Permission to republish or repurpose articles or portions of articles ): May 29, 2014 www.sciencemag.org (this information is current as of The following resources related to this article are available online at http://www.sciencemag.org/content/344/6187/1016.full.html version of this article at: including high-resolution figures, can be found in the online Updated information and services, http://www.sciencemag.org/content/suppl/2014/05/28/344.6187.1016.DC1.html can be found at: Supporting Online Material http://www.sciencemag.org/content/344/6187/1016.full.html#ref-list-1 , 20 of which can be accessed free: cites 67 articles This article http://www.sciencemag.org/cgi/collection/paleo Paleontology subject collections: This article appears in the following registered trademark of AAAS. is a Science 2014 by the American Association for the Advancement of Science; all rights reserved. The title Copyright American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the Science on May 29, 2014 www.sciencemag.org Downloaded from on May 29, 2014 www.sciencemag.org Downloaded from on May 29, 2014 www.sciencemag.org Downloaded from on May 29, 2014 www.sciencemag.org Downloaded from on May 29, 2014 www.sciencemag.org Downloaded from

Upload: d

Post on 25-Dec-2016

223 views

Category:

Documents


10 download

TRANSCRIPT

Page 1: Quaternary coral reef refugia preserved fish diversity

DOI: 10.1126/science.1249853, 1016 (2014);344 Science

et al.Loïc PellissierQuaternary coral reef refugia preserved fish diversity

This copy is for your personal, non-commercial use only.

clicking here.colleagues, clients, or customers by , you can order high-quality copies for yourIf you wish to distribute this article to others

  here.following the guidelines

can be obtained byPermission to republish or repurpose articles or portions of articles

  ): May 29, 2014 www.sciencemag.org (this information is current as of

The following resources related to this article are available online at

http://www.sciencemag.org/content/344/6187/1016.full.htmlversion of this article at:

including high-resolution figures, can be found in the onlineUpdated information and services,

http://www.sciencemag.org/content/suppl/2014/05/28/344.6187.1016.DC1.html can be found at: Supporting Online Material

http://www.sciencemag.org/content/344/6187/1016.full.html#ref-list-1, 20 of which can be accessed free:cites 67 articlesThis article

http://www.sciencemag.org/cgi/collection/paleoPaleontology

subject collections:This article appears in the following

registered trademark of AAAS. is aScience2014 by the American Association for the Advancement of Science; all rights reserved. The title

CopyrightAmerican Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by theScience

on

May

29,

201

4w

ww

.sci

ence

mag

.org

Dow

nloa

ded

from

o

n M

ay 2

9, 2

014

ww

w.s

cien

cem

ag.o

rgD

ownl

oade

d fr

om

on

May

29,

201

4w

ww

.sci

ence

mag

.org

Dow

nloa

ded

from

o

n M

ay 2

9, 2

014

ww

w.s

cien

cem

ag.o

rgD

ownl

oade

d fr

om

on

May

29,

201

4w

ww

.sci

ence

mag

.org

Dow

nloa

ded

from

Page 2: Quaternary coral reef refugia preserved fish diversity

9. K. M. Kahn, J. L. Cook, F. Bonar, P. Harcourt, M. Astrom,Sports Med. 27, 393–408 (1999).

10. L. C. Hughes, C. W. Archer, I. ap Gwynn, Eur. Cell. Mater. 9,68–84 (2005).

11. L. W. Jin et al., Proc. Natl. Acad. Sci. U.S.A. 100, 15294–15298(2003).

12. Y. Chen et al., Appl. Phys. Lett. 94, 053901 (2009).13. K. Kerkam, C. Viney, D. Kaplan, S. Lombardi, Nature 349,

596–598 (1991).14. For molecular solids, XB depends on the orientational

properties of the molecule containing the x-ray–absorbingatom, and in particular depends on the bonding environmentof this atom in the molecule. Here, we focus on XB studiesat the Br K edge for materials containing brominated organicmolecules. In this case, XB behavior can be rationalizedsimply on the basis of the orientational properties of theC–Br bonds (15, 16).

15. B. A. Palmer, A. Morte-Ródenas, B. M. Kariuki,K. D. M. Harris, S. P. Collins, J. Phys. Chem. Lett 2,2346–2351 (2011).

16. B. A. Palmer et al., J. Phys. Chem. Lett 3, 3216–3222(2012).

17. B. A. Collins et al., Nat. Mater. 11, 536–543 (2012).18. Y. Joly, S. P. Collins, S. Grenier, H. C. N. Tolentino,

M. De Santis, Phys. Rev. B 86, 220101 (2012).19. Materials and methods are available as supplementary

materials on Science Online.20. The spatial resolution of the XB images in the vertical

direction (~13 mm) is limited by the resolution of thecharge-coupled device–based detector, and the spatialresolution in the horizontal direction (~28 mm) is limitedby the penetration of the beam into the polarizationanalyzer [Si(555) reflection]. The latter could bereduced to less than 1 mm by using high-quality crystalsof heavier elements.

21. K. J. S. Sawhney et al., AIP Conf. Proc. 1234, 387–390(2010).

22. S. P. Collins et al., J. Phys. Conf. Ser. 425, 132015(2013).

23. C. Brouder, J. Phys. Condens. Matter 2, 701–738 (1990).24. S. P. Collins et al., J. Phys. Condens. Matter 14, 123–134

(2002).25. M.-H. Chao, B. M. Kariuki, K. D. M. Harris, S. P. Collins,

D. Laundy, Angew. Chem. Int. Ed. 42, 2982–2985(2003).

26. For c = 0°, the crystal c axis is horizontal (x-z plane), parallelto the linearly polarized incident x-ray beam.

27. B. A. Palmer, B. M. Kariuki, A. Morte-Ródenas, K. D. M. Harris,Cryst. Growth Des. 12, 577–582 (2012).

28. For BrCH/thiourea, the c axis is the tunnel axis of the thioureahost structure in both the high- and low-temperaturephases. With respect to the hexagonal unit cell (ah, bh, ch)of the high-temperature phase, the crystal orientation {c = 0°,ϕ = 0°} has the ch axis parallel to the laboratory x axis anda {100} plane perpendicular to the z axis. With respect tothe monoclinic unit cell (am, bm, cm) of the low-temperaturephase, in the crystal orientation {c = 0°, ϕ = 0°} the cmaxis is parallel to the laboratory x axis, the bm axis is parallel tothe z axis, and the projection of the am axis on the planeperpendicular to the cm axis [denoted proj(am)] isperpendicular to the x-z plane.

29. For ϕ = 0°, the bm axis of the crystal in the low-temperaturephase is parallel to the laboratory z axis. Hence, becausethe angle w (defined in Fig. 1D) is known (27) to be only~3.5°, the C–Br bonds in the major domain are very nearlyperpendicular to the direction of propagation of the incidentx-ray beam.

30. The changes of transmitted x-ray intensity as afunction of temperature in this material have beenrationalized previously (16) from XB studies using afocused x-ray beam.

31. H. Sirringhaus et al., Appl. Phys. Lett. 77, 406–408(2000).

32. H. Sirringhaus et al., Nature 401, 685–688 (1999).33. J. Stasiak, A. Zaffora, M. L. Constantino, A. Pandolfi,

G. D. Moggridge, Func. Mater. Lett. 3, 249–252 (2010).34. In contrast, other techniques (35–39) for imaging materials

that use incident x-ray radiation (such as scanning x-raymicroscopy and x-ray topography) generally involve scanninga focused x-ray beam across the material (leading to theconstruction of a spatially resolved image through theanalysis of the interaction of the beam with the material ateach position of the beam). The time required to record a

single image in XBI is clearly much faster than would be thecase with a scanning probe. One consequence is that theoverall radiation dose received by the sample should belower in the case of XBI, suggesting that XBI may beadvantageous in studying materials that are susceptible toradiation damage.

35. H. Ade, B. Hsiao, Science 262, 1427–1429 (1993).36. D. Sayre, H. N. Chapman, Acta Crystallogr. A 51, 237–252

(1995).37. D. K. Bowen, B. K. Tanner, High Resolution X-ray

Diffractometry and Topography (Taylor & Francis, London, UK,1998).

38. M. Howells, C. Jacobsen, T. Warwick, A. Van den Bos, inScience of Microscopy, P. W. Hawkes, J. C. H. Spence, Eds.(Springer, New York, 2007), pp. 835–926.

39. P. Thibault et al., Science 321, 379–382 (2008).

ACKNOWLEDGMENTS

We are grateful to Diamond Light Source for the award ofbeam-time for experiments on beamline B16. We thank theEngineering and Physical Sciences Research Council (studentshipsto B.A.P. and G.R.E.-G.) and Cardiff University for financialsupport.

SUPPLEMENTARY MATERIALS

www.sciencemag.org/content/344/6187/1013/suppl/DC1Materials and MethodsFigs. S1 to S3Movies S1 to S7

18 March 2014; accepted 29 April 201410.1126/science.1253537

MARINE BIOGEOGRAPHY

Quaternary coral reef refugiapreserved fish diversityLoïc Pellissier,1,2 Fabien Leprieur,3 Valeriano Parravicini,4,5 Peter F. Cowman,6

Michel Kulbicki,4 Glenn Litsios,7,8 Steffen M. Olsen,9 Mary S. Wisz,2,10

David R. Bellwood,11 David Mouillot3,11*

The most prominent pattern in global marine biogeography is the biodiversity peak inthe Indo-Australian Archipelago. Yet the processes that underpin this pattern are stillactively debated. By reconstructing global marine paleoenvironments over the past3 million years on the basis of sediment cores, we assessed the extent to which Quaternaryclimate fluctuations can explain global variation in current reef fish richness. Comparingglobal historical coral reef habitat availability with the present-day distribution of 6316reef fish species, we find that distance from stable coral reef habitats during historicalperiods of habitat loss explains 62% of the variation in fish richness, outweighingpresent-day environmental factors. Our results highlight the importance of habitatpersistence during periods of climate change for preserving marine biodiversity.

Tropical marine biodiversity shows a uniquelongitudinal pattern with a peak of speciesrichness in the Indo-Australian Archipel-ago (IAA) (1, 2). With their biological andstructural complexity, coral reefs support

the world’s greatest diversity of marine fishes(3–5). Reef-building corals track well-definedconditions of sea surface temperature and light(6) and are thus particularly sensitive to chan-ges in climate and sea level. On short temporaland small spatial scales, coral assemblagesexhibit highly dynamic fluctuations in species com-position and abundance, with species-specificresponses to disturbances (7, 8). At longer timescales, fossil records show that coral reefs mayhave experienced dramatic contractions in re-sponse to environmental shifts. Themost strikingexample is the last interglacial period, ~125,000years ago, when a rise in sea surface temperaturecaused an equatorial retraction of coral reefs witha rapid loss of marine biodiversity (9). Coldertemperatures and sea level drops have also beenresponsible for massive coral habitat loss in thepast, with many coral reefs arising after the lastglacial maximum (10). Given the dependency ofmost reef fishes on coral reef habitat (11, 12),historical climatic oscillations are likely to haveaffected fish persistence and thus current bio-diversity patterns.The Quaternary period (2.6 million years ago

to present) is characterized by at least 30 glacial-interglacial cycles of repeated global cooling andwarming with consequences for reef habitat

RESEARCH | REPORTS

1University of Fribourg, Department of Biology, Chemin duMusée 10, CH-1700 Fribourg, Switzerland. 2Department ofBioscience, Aarhus University, 8000 C Aarhus, Denmark.3Laboratoire Ecologie des Systèmes Marins Côtiers UMR5119, CNRS, Institut de Recherche pour le Développement(IRD), Institut Français de Recherche pour l’Exploitation de laMer, UM2, UM1, cc 093, Place E. Bataillon, FR-34095Montpellier Cedex 5, France. 4IRD, UR 227 CoReUs, LABEX(Laboratoire d’Excellence) Corail, Laboratoire Arago, BoîtePostale 44, FR-66651 Banyuls/mer, France. 5CESAB (Centrede Synthèse et d’Analyse sur la Biodiversité)–FRB(Fondation pour la Recherche sur la Biodiversité), ImmeubleHenri Poincaré, Domaine du Petit Arbois, FR-13857 Aix-en-Provence cedex 3, France. 6Centre for Macroevolution andMacroecology, Research School of Biology, AustralianNational University, Canberra, ACT 0200, Australia.7Department of Ecology and Evolution, Biophore Building,University of Lausanne, 1015 Lausanne, Switzerland. 8SwissInstitute of Bioinformatics, Quartier Sorge, 1015 Lausanne,Switzerland. 9Center for Ocean and Ice, DanishMeteorological Institute, Lyngbyvej 100, 2100 Copenhagen,Denmark. 10Department of Ecology and Environment, DHIWater and Environment, 2970 Hørsholm, Denmark.11Australian Research Council Centre of Excellence for CoralReef Studies, and School of Marine and Tropical Biology,James Cook University, Townsville, QLD 4811, Australia.*Corresponding author. E-mail: [email protected]

1016 30 MAY 2014 • VOL 344 ISSUE 6187 sciencemag.org SCIENCE

Page 3: Quaternary coral reef refugia preserved fish diversity

availability. Stable coral reef habitats over geo-logical time may have promoted fish biodiversityby acting as (i) refugia, which preserved speciesfrom extinction because of habitat loss (4, 13); (ii)sources for the recolonization of unstable areasduring more favorable periods (14, 15); and (iii)evolutionary cradles with high speciation rates(16). Given these combined benefits, Quater-nary coral reef refugia should have left theirimprint on current richness patterns of coral reeffishes worldwide. To explore the influence of en-vironmental history on global fish diversity pat-terns on tropical reefs, we identified the putativelocations of refugia, defined as habitat suitablefor corals during cold periods, by reconstructingcoral reef paleodistributions during the Quater-nary. By building on sea surface temperatureand sea level paleoconditions inferred from sedi-ment cores (17, 18) to bind the coral reef environ-mental envelope (figs. S1 and S2), we mappedthe paleodistribution of this habitat for thepast three million years with a temporal res-olution of 1000 years (Fig. 1A) by using an ac-curate model [95% of correct classification (fig.S3)]. For each current reef, isolation from refugiawas computed as the sea distance to historicalcoral reef habitats across the glaciation cycles(Fig. 1B). We also mapped, at 5°-by-5° resolution,the global distribution of fish species richnessby using the geographic range of 6316 tropicalreef fishes (Fig. 1C). We then predicted fish rich-ness patterns from historical (past coral reef areaand isolation from refugia) and contemporary(mean sea surface temperature, coral reef area,and isolation) factors by using a set of bivariateand multivariate linear regression models in-cluding quadratic terms to account for non-linear relationships.We found that isolation fromQuaternary refu-

gia was the primary driver of reef fish richness(Fig. 2A) and that its effect was far greater thanall other factors, including past and current coralreef area, isolation, and sea surface temperature(table S1). Areas closer to Quaternary refugia dis-play higher fish richness (R2 = 0.62; P < 0.0001)(Figs. 1 and 2A), emphasizing the crucial role ofstable coral reef habitat during the Quaternary.When considering contemporary factors, neitherthe sea surface temperature (R2 = 0.25; P <0.0001) nor the level of isolation of coral reefhabitats (R2 = 0.30; P < 0.0001) or even the coralreef area (R2 = 0.33; P < 0.0001) provided near orexceeding explanatory power to isolation fromQuaternary refugia (table S1). These observationsare supported by two complementary analyses.First, isolation from Quaternary refugia receivedthe highest support over all subset models mix-ing historical and contemporary factors (tableS2). Second, when partitioning the explained var-iance of fish richness (R2 = 0.73) among historicaland contemporary factors included in themodel,isolation from Quaternary refugia showed thestrongest independent effect, with a higher pro-portion of explained variance (24.4%) than cur-rent coral reef area, coral reef isolation, and seasurface temperature combined (15.5%). Further-more, the explanatory power of historical extent

of coral reef habitat on fish richness peakedduring time periods when sea temperature wasthe lowest, causing the strongest coral reef habi-tat contractions (R2 = 0.45, P < 0.0001) (figs. S4and S5). Similar results are obtained when ex-cluding the tropical Eastern Pacific and Atlanticbasins that display the highest levels of isola-tion from refugia and the lowest extents of coralreef habitat during the cold periods comparedwith those located in the Indo-Pacific, suggestingthat our findings are not biased by a basin effect(table S3 and figs. S6 and S7). Taken together, ourresults highlight how areas that retained suitablecoral reef habitat over geological time served asrefugia, buffering species from extinction byminimizing stochastic processes leading to pop-ulation decline (19, 20).The impact of past habitat availability on cur-

rent fish richness patterns should also depend onrecolonization ability, mainly through larval disper-sal that varies across families (21). Among the threefamilies investigated (Pomacentridae, damselfishes;Labridae, wrasses; Chaetodontidae, butterflyfishes),damselfishes should show the strongest response toisolation from refugia, given their low swimmingability during the late pelagic stage and shorter

pelagic larval duration, compared with wrassesand butterflyfishes (21). We estimated segmentbreakpoints in the regressionmodels linking fishrichness to the isolation fromQuaternary refugiato test for a family-specific response (Fig. 2, B toD). Isolation from refugia was closely related tofish richness for the three families, suggestingcommon drivers (Fig. 2 and table S4), but theirbreaking points differed (fig. S8). As expectedfrom their ecological characteristics and larvaldispersal capacity (21), the damselfishes show abreak point in fish richness at a lower level ofisolation from refugia (46.1 km) compared withbutterflyfishes (396.7 km) and wrasses (291.3 km).Lending additional support to this pattern, theeffect of past extent of coral reef habitat is abetter predictor of richness for damselfishes thanfor the two other families (table S4). Indeed,damselfishes richness is especially concentratedin the Indo-Pacific, which maintained extensiverefugia during the Quaternary.Historical barriers, such as those created by

sea level drops during the Quaternary, may haveplayed important roles in the isolation of pop-ulations by cutting off local sea basins (22, 23).Paleohabitat models suggest that not only were

Fig. 1. Location of coral reefs, past isolation, and current fish richness. Maps of (A) the coral reefarea per 5°-by-5° cell averaged for the periods of marked coral reef contraction, as characterized by lowersea surface temperature and sea level (square degree); (B) standardized isolation from stable coral reefareas across the Quaternary (kilometers); and (C) current global richness of reef fishes (number ofspecies).

RESEARCH | REPORTS

SCIENCE sciencemag.org 30 MAY 2014 • VOL 344 ISSUE 6187 1017

Page 4: Quaternary coral reef refugia preserved fish diversity

the Atlantic and Indo-Pacific oceans isolated fromeach other but that coral reefs within the Indo-Pacific were isolated in refugia such as the Red

Sea, Madagascar, and Maldives, along with mul-tiple small refugia within the IAA (Fig. 3). Inparticular, we found an increased spatial frag-

mentation of coral reef habitat over time fromthe onset of glaciations in the Indo-Pacific ocean(landscape division index, R2 = 0.15, P < 0.0001)(Fig. 3). Fragmentation was highest during theperiods with the coldest temperatures (R2 =0.51, P < 0.0001) (fig. S9). Our dated phyloge-nies indicate that a large proportion of fisheswithin the target families arose in the past 3million years (percentage of species with an ageof divergence from the most closely relatedsister species <3 Ma for wrasses is 19%; dam-selfishes, 31%; butterflyfishes, 65%) (Fig. 3).The number of recently diverged species (<3Ma)was highest in proximity to refugia where thesespecies could have arisen (wrasses, R2 = 0.61 andP < 0.0001; butterflyfishes, R2 = 0.65 and P <0.0001; damselfishes, R2 = 0.57 and P < 0.0001).Our results provide evidence for the role of dis-connected but stable habitat area in promotingspecies diversification during the Quaternary,especially in the Indo-Pacific (24).High extinction and low speciation rates in

areas outside putative refugia can reduce speciesrichness and should also affect the age of lineagesrepresented in species assemblages (25). Refugiaare expected to preserve species from extinctionand should harbor the oldest species. In contrast,unstable areas are likely to harbor younger col-onists, resulting in a narrower range of agesbecause they lack older species. Consistent withthis hypothesis, the difference between the 95thand 5th percentiles of species age distribution islarger in refugia for all three families (wrasses,R2 = 0.22, P < 0.0001; butterflyfishes, R2 = 0.32,P < 0.0001; and damselfishes, R2 = 0.53, P <0.0001) (Fig. 4) without any bias related tovariation in species richness (fig. S10). The effectof isolation from refugia is weaker for thewrasses than for the other two families (Fig. 4).The oldest wrasses occur both in the Indo-Pacificand in the Atlantic, the latter resulting fromAtlantic colonization from the west Tethys Sea

Fig. 2. Relationship between the standardized isolation from stable coral reef areas across theQuaternary and total richness of reef fishes. Shown is the total reef fish richness (A) as well as richnessof three families: wrasses (B), butterflyfishes (C), and damselfishes (D). [Photo credits: J. P. Krajewski (B)and (D) and S. Gingins (C)]

Fig. 3. Reef paleodistribution and species age. Proj-ected coral reef habitat for two time periods (yellow) basedon historical sea surface temperature and sea level at –21thousand years (Ky) (A) and –896 Ky (B). Expert-delimitedecoregions based on faunal dissimilarity are shown in shadesof blue. The coral reef area for each time step was used tocompute the change in habitat fragmentation through time,which is represented as the yellow line in (C). Also shown inblack is the histogram of species age for wrasses, butterfly-fishes, and damselfishes.

RESEARCH | REPORTS

1018 30 MAY 2014 • VOL 344 ISSUE 6187 sciencemag.org SCIENCE

Page 5: Quaternary coral reef refugia preserved fish diversity

(3, 4). Because Atlantic lineages are less associatedwith coral reef habitats (3, 4), instability during theQuaternary likely had a lower impact on thepersistence of wrasses. In support of this result,the wrasses have exhibited relatively few new spe-cies in the past 3million years (Fig. 3), suggesting aless intense effect of habitat fragmentation duringthe Quaternary.Our results highlight the central role of coral

reef refugia during Quaternary climatic fluctua-tions and how isolation from refugia has modu-lated fish richness patterns. The distance fromthe Indo-Pacific center was found to be a majordeterminant of fish richness (26). The Indo-Pacificmaintained extensive coral reef refugia duringcold periods with low sea level stands (Fig. 1A), inareas including the IAA, Maldives, Madagascar,and Red Sea (Fig. 3). These areas thus appear tohave acted as centers of survival, as previouslysuggested (27, 28). By contrast, in the Atlantic,only very limited areas were suitable for coralreefs during cold periods (Fig. 1A), implying adegradation of Caribbean coral reefs after theonset of glaciation. This may explain the rela-tively weak association of Caribbean fishes withcoral reef habitats (29) and the high extinctionrates around 2 to 1 Ma observed in near-shoreenvironments (30). Paralleling results for sub-tropical rainforest (31), we demonstrate thathistorical habitat availability in coral reefs isas important as current habitat extent in ex-plaining observed distributions of fish speciesrichness. Our results suggest that the possible“cradle” effect of coral reefs may have arisen fromincreased fragmentation during episodic coldevents, especially in the IAA (Fig. 3). Quater-nary climatic fluctuations have left theirmark oncontemporary patterns of reef fish biodiversitythrough historical shifts in habitat availabilityand isolation.Examining how coral reefs have changed in

the past may give new insight into understand-ing how reef species might respond to globalchange (32). Our results suggest that current reef

fish biodiversity can be primarily explained bypast habitat availability. This finding has impor-tant implications for conservation of coral reefsworldwide under ongoing climate change. Mostnotably, the warm refugia that protected speciesin the past may in turn be the first to be threat-ened by future warming (33). Ideally, manage-ment strategies should focus on the protection ofcoral reefs over large areas that maintain cor-ridors of suitable habitat that allow the resilienceof fish biodiversity through connectivity fromhistorical refugia. Our results emphasize the strongrelationship between reef fish biodiversity, pasthabitat shifts, the role of habitat conservationunder climate change, and, more generally, therole of historical habitat shift in shaping the di-versity of life we observe today.

REFERENCES AND NOTES

1. D. R. Bellwood, T. P. Hughes, Science 292, 1532–1535(2001).

2. W. Renema et al., Science 321, 654–657 (2008).3. S. A. Price, R. Holzman, T. J. Near, P. C. Wainwright, Ecol. Lett.

14, 462–469 (2011).4. P. F. Cowman, D. R. Bellwood, J. Biogeogr. 40, 209–224

(2013).5. V. Parravicini et al., Ecography 36, 1254–1262 (2013).6. J. A. Kleypas et al., Am. Zool. 39, 146 (1999).7. J. H. Connell, T. P. Hughes, C. C. Wallace, Ecol. Monogr. 67,

461–488 (1997).8. T. P. Hughes et al., Curr. Biol. 22, 736–741 (2012).9. W. Kiessling, C. Simpson, B. Beck, H. Mewis,

J. M. Pandolfi, Proc. Natl. Acad. Sci. U.S.A. 109,21378–21383 (2012).

10. J. E. N. Veron, M. Stafford-Smith, Corals of the World(Australian Institute of Marine Science, Townsville, Australia,2000).

11. M. J. Paddack et al., Curr. Biol. 19, 590–595 (2009).12. M. C. Bonin, G. R. Almany, G. P. Jones, Ecology 92, 1503–1512

(2011).13. G. Paulay, Paleobiology 16, 415–434 (1990).14. A. C. Carnaval, M. J. Hickerson, C. F. Haddad, M. T. Rodrigues,

C. Moritz, Science 323, 785–789 (2009).15. B. Sandel et al., Science 334, 660–664 (2011).16. D. D. McKenna, B. D. Farrell, Proc. Natl. Acad. Sci. U.S.A. 103,

10947–10951 (2006).17. K. G. Miller et al., Science 310, 1293–1298 (2005).18. T. D. Herbert, L. C. Peterson, K. T. Lawrence, Z. Liu, Science

328, 1530–1534 (2010).19. M. L. Rosenzweig, Species Diversity in Space and Time

(Cambridge Univ. Press, Cambridge, 1995).

20. S. L. Chown, K. J. Gaston, Trends Ecol. Evol. 15, 311–315(2000).

21. O. J. Luiz et al., Proc. Natl. Acad. Sci. U.S.A. 110, 16498–16502(2013).

22. J. W. McManus, “Marine speciation, tectonics, and sea-levelchanges in Southeast Asia,” in Proceedings of the FifthInternational Coral Reef Congress, C. Gabrie, B. Salvat, Eds.(International Coral Reef Symposium, Penang, Malaysia, 1985),vol. 4, pp. 133–138.

23. D. C. Potts, in Proceedings of the Fifth International CoralReef Congress, C. Gabrie, B. Salvat, Eds. (InternationalCoral Reef Symposium, Penang, Malaysia, 1985), vol. 4,pp. 127–132.

24. A. J. Kohn, in Proceedings of the Fifth International CoralReef Congress, C. Gabrie, B. Salvat, Eds. (InternationalCoral Reef Symposium, Penang, Malaysia, 1995), vol. 4,pp. 139–144.

25. J. Fjeldså, J. C. Lovett, Biodivers. Conserv. 6, 325–346 (1997).26. C. Mora, P. M. Chittaro, P. F. Sale, J. P. Kritzer, S. A. Ludsin,

Nature 421, 933–936 (2003).27. P. H. Barber, D. R. Bellwood, Mol. Phylogenetics Evol. 35,

235–253 (2005).28. D. R. Bellwood, C. P. Meyer, J. Biogeogr. 36, 569–576 (2009).29. D. R. Bellwood, P. C. Wainwright, in Coral Reef Fishes:

Dynamics and Diversity in a Complex Ecosystem, P. F. Sale, Ed.(Academic Press, San Diego, CA, 2002).

30. A. O’Dea et al., Proc. Natl. Acad. Sci. U.S.A. 104, 5501–5506(2007).

31. C. H. Graham, C. Moritz, S. E. Williams, Proc. Natl. Acad.Sci. U.S.A. 103, 632–636 (2006).

32. J. M. Pandolfi, S. R. Connolly, D. J. Marshall, A. L. Cohen,Science 333, 418–422 (2011).

33. C. Mora et al., PLOS Biol. 11, e1001682 (2013).

ACKNOWLEDGMENTS

This study was supported by grants from the Danish Councilfor Independent Research no. 12-126430 to L.P., Marie CurieIOF-GA-2009-236316 to D.M., FRB CESAB–General Approach toSpecies-Abundance Relationships in a context of global change,reef fish species as a model, and the Australian Research Council.We thank three anonymous reviewers for valuable commentson the manuscript. We thank J. P. Krajewski and S. Ginginsfor the fish images. Data are available in the supplementarymaterials.

SUPPLEMENTARY MATERIALS

www.sciencemag.org/content/344/6187/1016/suppl/DC1Materials and MethodsFigs. S1 to S14Tables S1 to S4References (34–80)Database S1

17 December 2013; accepted 24 April 201410.1156/science.1249853

Fig. 4. Isolation distance and species age. (A to C) Relationship between the standardized isolation from stable coral reef areas across the Quaternary(kilometers) and the difference between the 95th and 5th percentile of species age in assemblages in eachcell.Cells closer to refugia during theQuaternary have alarger age range because they contain both older and younger species.

RESEARCH | REPORTS

SCIENCE sciencemag.org 30 MAY 2014 • VOL 344 ISSUE 6187 1019