This article corresponds to Huang, D., E. E. Goldberg, L. M. Chou, and K. Roy. 2018. The origin and evolution of coral species richness in a marine biodiversity hotspot. Evolution.https://doi.org/10.1111/evo.13402

Cass, Susannah

Dodsworth, Steven

Pérez-Escobar, Oscar Alejandro

Evolution

English

Oscar Alejandro Pérez‐Escobar

Susannah Cass

Steven Dodsworth

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Digest: Drivers of coral diversification in a major marine biodiversity hotspot*

Dodsworth, S.

Pérez-Escobar, O. A.

Cass, S.

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Drivers of coral diversification in a major marine biodiversity hotspot.

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DIGESTSdoi:10.1111/evo.13419Digest: Drivers of coral diversificationin a major marine biodiversity hotspot∗Oscar Alejandro Pérez-Escobar,1 Susannah Cass,2 and Steven Dodsworth1,31Royal Botanic Gardens, Kew, Richmond TW9 3AB, Surrey, United Kingdom2Trinity Centre for Biodiversity Research, Trinity College Dublin, Dublin 2, Ireland3E-mail: s.dodsworth@kew.orgReceived December 4, 2017Accepted December 18, 2017Coral reefs are of great ecological importance for marine wildlife(Knowlton 2001); despite occupying less than 0.1 percent of thesurface area of the world’s oceans, they provide habitats for at leasta quarter of marine species (Spalding and Grenfell 1997). They arefragile ecosystems, under threat from numerous stresses includ-ing climate change, ocean acidification, and destructive fishingpractices (Pandolfi 2003). Despite their great ecological impor-tance, relatively little is known about the evolution of coral reefs.The mode and tempo of evolution in coral reef systems are poorlyunderstood, with data lacking on the origin and diversification ofcoral hotspots (Huang and Roy 2015).In this issue, Huang et al. (2017) utilize a solid phyloge-netic framework based on two sets of trees of coral species: onethat uses earlier supertree studies incorporating published molec-ular data (seven mitochondrial DNA markers) and morphologicaltrees, and one that uses an expanded molecular dataset (sevenmitochondrial plus two nuclear DNA regions). In both cases, fos-sil calibrations were used to date the trees. Using these differentphylogenetic datasets, they tested the mode of diversification inthe Indo-Pacific Coral Triangle (CT) biodiversity hotspot to testcompeting hypotheses regarding the temporal dynamics of coralspecies richness.The Coral Triangle is a geographic area encompassing theoceans around Malaysia, the Phillippines, Indonesia, Timor-Leste, Papua New Guinea, and the Solomon Islands. Phyloge-netic analyses indicate that diversity within the CT was drivenmostly by range expansions of lineages that originated outsidethe CT. Speciation rates within the CT region itself were lowerthan surrounding regions, as endemic CT lineages were found to∗This article corresponds to Huang, D., E. E. Goldberg, L. M. Chou, andK. Roy. 2018. The origin and evolution of coral species richness in a marinebiodiversity hotspot. Evolution. https://doi.org/10.1111/evo.13402.be older than widespread lineages or those found outside the CT.The drivers of these range shifts are currently unknown, but suchshifts could be underpinned by time-dependent variables includ-ing changing climatic conditions, as observed in plant (Antonelliet al. 2010; Pérez-Escobar et al. 2017a) and insect (Condamineet al. 2012) lineages.Diversification patterns of corals in the CT resemble the di-versification dynamics of other eukaryotic lineages that are highlydiverse in biodiversity hotspots. For example, in Andean orchids(Pérez-Escobar et al. 2017b), asynchronous migrations from ad-jacent regions followed by rapid diversification have led to ex-tremely high species diversity in montane areas. This contradictsthe museum hypothesis, whereby species accumulate at a constantrate over time with little extinction. Huang et al.’s findings positmany puzzling questions for the origin of biodiversity hotspotsmore generally. For the specific case of the CT, when in timedid the wave of migrants move into the CT? Were migrationsand recolonizations asynchronous or did they happen simultane-ously? The data generated by the authors provide a solid phylo-genetic framework to address these questions, and will be helpfulto understand in detail the temporal evolutionary dynamics ofthe CT.Macroevolutionary analyses (Fig. 1A) on the scleractinianphylogeny of Huang et al. (2017) reveal multiple, asynchronousshifts in diversification rates and a constant increase in net diversi-fication rates through time (Fig. 1D). Additionally, they revealedoverall lower tip speciation and extinction rates of endemic CTlineages (Fig. 1B and C) compared with species distributed out-side the CT, but also those that are widespread (occurring in theCT and outside). Surprisingly, most of the diversification rateshifts are concentrated toward the Cenozoic, and across cladesincluding both widespread and endemic CT species.4 0 6C© 2018 The Author(s). Evolution C© 2018 The Society for the Study of Evolution.Evolution 72-2: 406–408DIGESTFigure 1. (A) Diversification rate plot (phylorate) of scleractinian reef coral lineages showing changes in diversification rates throughtime (best configuration shift identified by BAMM, and inferred from a maximum clade credibility tree with common ancestor heights;(Rabosky 2014)). Cold colors represent slower diversification rates, while warm colors indicate faster diversification rates. Red circleson branches represent locations of rate shifts. Geographical ranges (i.e., species endemic to CT vs taxa distributed outside the CT, orwidespread) are shown as horizontal bars in front of the terminals. Family members of Scleractinia are color coded: Acr.: Acroporidae; Eup.:Euphylliidae; Aga.: Agariciidae; Side.: Siderastreidae; Astr.: Astrocoeniidae; Pori.: Poritidae; Den.: Dendrophylliidae; Mer.: Merulinidae;Lobo.: Lobophylliidae; Muss.: Mussidae; Ples.: Plesiastreidae; Ocu.: Oculinidae; Mea.: Meandrinidae; Fung.: Fungiidae; Cosci.: Coscinaraei-dae; Cary.: Caryophylliidae; Poll.: Pocilloporidae. Tip speciation (B) and extinction (C) rates of reef coral lineages per geographical range(coding sensu Hughes et al. 2013—see Huang et al. supporting online material). Mean rate values are indicated with a pink bar. Note thelower speciation and extinction rates in coral species endemic to CT; diversification rates of widespread and outsider CT taxa, however,are very similar. (D) Net diversification rates of sclerictinian reef coral lineages through time shows a constant increase of rates, with anacceleration near the K/T boundary.EVOLUTION FEBRUARY 2018 4 0 7DIGESTThis study paves the way for future research where the tempoof diversification of CT lineages can be further investigated. Thiswill help us to understand how diversification rates in coral reeflineages have responded to past climatic and geological changes,as reported in alternative eukaryote lineages (Condamine et al.2013; Lagomarsino et al. 2016). More importantly, future re-search will enable the understanding of changes in coral reefspecies-pump and sink area dynamics through time. Lastly, Huanget al. (2017) highlight the importance of such evolutionary studiesfor conservation efforts, as the regions surrounding biodiversityhotspots may be as important to conserve as the hotspots them-selves.LITERATURE CITEDAntonelli, A., C. F. Verola, C. N. Parisod, and A. L. S. Gustafsson. 2010.Climate cooling promoted the expansion and radiation of a threatenedgroup of South American orchids (Epidendroideae: Laeliinae). Biol. J.Linn. Soc. 100:597–607.Condamine, F. L., J. Rolland, and H. Morlon. 2013. Macroevolutionary per-spectives to environmental change. Ecol. Lett. 16:72–85.Condamine, F. L., F. A. H. Sperling, N. Wahlberg, J. Y. Rasplus, and G. J.Kergoat. 2012. What causes latitudinal gradients in species diversity?Evolutionary processes and ecological constraints on swallowtail biodi-versity. Ecol. Lett. 15:267–277.Huang, D., and K. Roy. 2015. The future of evolutionary diversity in reefcorals. Philos. Trans. R. Soc. B Biol. Sci. 370:20140010–20140010.Huang, D., E. E. Goldberg, L. M. Chou, and K. Roy. 2017. The origin andevolution of coral species richness in a marine biodiversity hotspot.Evolution 72:288–302.Knowlton, N. 2001. The future of coral reefs. Proc. Natl. Acad. Sci. USA98:5419–5425.Lagomarsino, L., F. L. Condamine, A. Antonelli, A. Mulch, and C. C. Davis.2016. The abiotic and biotic drivers of rapid diversification in Andeanbellflowers (Campanulaceae). New Phytol. 210:1430–1432.Pandolfi, J. M. 2003. Global trajectories of the long-term decline of coral reefecosystems. Science 301:955–958.Pérez-Escobar, O. A., G. Chomicki, F. L. Condamine, J. M. De Vos, A. C. Mar-tins, E. C. Smidt, B. Klitgård, G. Gerlach, and J. Heinrichs. 2017a. Mul-tiple geographical origins of environmental sex determination enhancedthe diversification of Darwin’s favourite orchids. Sci. Rep. 7:12878.Pérez-Escobar, O. A., G. Chomicki, F. L. Condamine, A. P. Karremans, D.Bogarı́n, N. J. Matzke, D. Silvestro, and A. Antonelli. 2017b. Recentorigin and rapid speciation of Neotropical orchids in the world’s richestplant biodiversity hotspot. New Phytol. 215:891–905.Rabosky, D. L. 2014. Automatic detection of key innovations, rate shifts, anddiversity-dependence on phylogenetic trees. PLoS One 9:e89543.Spalding, M. D., and A. M. Grenfell. 1997. New estimates of global andregional coral reef areas. Coral Reefs 16:225–230.Associate Editor: K. MooreHandling Editor: M. NoorSUBMIT A DIGESTDigests are short (500 word), news articles about selectedoriginal research included in the journal, written by studentsor postdocs. These digests are published online and linked totheir corresponding original research articles. For instructions onDigests preparation and submission, please visit the followinglink: https://sites.duke.edu/evodigests/.4 0 8 EVOLUTION FEBRUARY 2018

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