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Phylogenetic insights into the history and diversification of fishes on reefs

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Abstract

Studies of the phylogenetic history of fishes on reefs and the impact of reefs on fish diversification have, to date, been limited to relatively small clades. We take advantage of a recent multi-locus, time-calibrated phylogeny of acanthomorph fishes and a broad-scale morphological dataset of body shape in reef acanthomorphs to explore the history and diversification of fish on reefs at the family level. We find that no reef family exhibits exceptional species diversity for their stem age and some, such as Aulostomidae, Zanclidae, Menidae, and Triodontidae may in fact be species poor. The inferred history of reef colonization is highly dependent on how a reef family is defined; one classification scheme raises the possibility that most modern acanthomorph families originated on reefs. We find that most reef families occupy surprisingly distinct regions of morphospace and yet, some of the most diverse reef families occupy central and highly overlapping positions within the body shape morphospace. To the extent that proximity in morphospace reflects ecological similarity, these results imply that most reef fish families have diversified in adaptive zones away from other families. In contrast, a few of the most successful (e.g., Labridae and Pomacentridae) have achieved dominance while potentially facing stronger interactions with other lineages. Finally, we find no relationship between species diversity and body shape diversity. Assuming neither are diversity dependent, this result suggests that morphological and ecological diversification within families of reef fish may not be linked to the accumulation of species. Time-calibrated phylogenies provide the means for generating a greater understanding of the macroevolutionary processes influencing reef fish diversification, but we are currently limited by the lack of robust crown-group ages for many reef fish families.

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References

  • Adams DC, Otarola-Castillo E (2013) geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol Evol 4:393–399

    Article  Google Scholar 

  • Alfaro M, Santini F, Brock CD (2007) Do reefs drive diversification in marine teleosts? Evidence from the pufferfish and their allies (Order Tetraodontiformes). Evolution 61:2104–2126

    Article  PubMed  Google Scholar 

  • Bellwood DR (1996) The Eocene fishes of Monte Bolca: the earliest coral reef fish assemblages. Coral Reefs 15:11–19

    Article  Google Scholar 

  • Bellwood DR (1998) What are reef fishes? - Comment on the report by D. R. Robertson: Do coral-reef fish faunas have a distinctive taxonomic structure? Coral Reefs 17:187–189

    Article  Google Scholar 

  • Bellwood DR (2003) Origins and escalation of herbivory in fishes: a functional perspective. Paleobiology 29:71–83

    Article  Google Scholar 

  • Bellwood DR, Wainwright PC (2002) The history and biogeography of fishes on coral reefs. In: Sale PF (ed) Coral reef fishes: diversity and dynamics in a complex ecosystem. Academic Press, Boston, pp 5–32

    Chapter  Google Scholar 

  • Betancur RR, Broughton RE, Wiley EO, Carpenter K, Lopez JA, Li C, Holcroft NI, Arcila D, Sanciangco M, Cureton JCI, Zhang F, Buser T, Campbell MA, Ballesteros JA, Roa-Varon A, Willis S, Borden WC, Rowley T, Reneau PC, Hough DJ, Lu G, Grande T, Arratia G, Orti G (2013) The tree of life and a new classification of bony fishes. PLoS Currents 5: ecurrents.tol.53ba26640df0ccaee75bb165c8c26288

  • Bivand R, Lewin-Koh N (2014) maptools: Tools for reading and handling spatial objects. R package version 0.8-30. http://CRAN.R-project.org/package=maptools

  • Bivand R, Rundel C (2014) rgeos: Interface to Geometry Engine - Open Source (GEOS). R package version 0.3-6. http://CRAN.R-project.org/package=rgeos

  • Boettiger C, Lang DT, Wainwright PC (2012) rfishbase: exploring, manipulating and visualizing FishBase data from R. Fish Biol 81:2030–2039

    Article  CAS  Google Scholar 

  • Bollback JP (2006) SIMMAP: Stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7:88

    Article  PubMed Central  PubMed  Google Scholar 

  • Calenge C (2006) The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519

    Article  Google Scholar 

  • Claverie T, Wainwright PC (2014) A morphospace for coral reef fishes: elongation is the dominant axis of body shape evolution. PLoS One 9:e112732

    Article  PubMed Central  PubMed  Google Scholar 

  • Cowman PF, Bellwood DR (2011) Coral reefs as drivers of cladogenesis: expanding coral reefs, cryptic extinction events, and the development of biodiversity hotspots. J Evol Biol 24:2543–2562

    Article  CAS  PubMed  Google Scholar 

  • Eschmeyer WN (2012) Catalog of fishes. California Academy of Sciences (http://research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp)

  • Friedman M, Johnson G (2005) A new species of Mene (Perciformes: Menidae) from the Paleocene of South America, with notes on paleoenvironment and a brief review of menid fishes. J Vert Paleontol 25:770–783

    Article  Google Scholar 

  • Froese R, Pauly D (2013) FishBase. World Wide Web electronic publication. http://www.fishbase.org

  • Harmelin-Vivien ML (2002) Energetics and fish diversity on coral reefs. In: Sale PF (ed) Coral reef fishes. Dynamics and diversity in a complex ecosystem. Academic Press, Boston, pp 265–274

    Chapter  Google Scholar 

  • Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131

    Article  CAS  PubMed  Google Scholar 

  • Herler J, Munday PL, Hernaman V (2011) Gobies on coral reefs. In: Patzner RA, Van Tassell JL, Kovacic M, Kapoor BG (eds) The biology of gobies. Science Publishers, New Hampshire, pp 493–539

    Chapter  Google Scholar 

  • Kiessling W, Simpson C, Foote M (2010) Reefs as cradles of evolution and sources of biodiversity in the Phanerozoic. Science 327:196–198

    Article  CAS  PubMed  Google Scholar 

  • Magallón S, Sanderson MJ (2001) Absolute diversification rates in angiosperm clades. Evolution 55:1762–1780

    Article  PubMed  Google Scholar 

  • Near TJ, Dornburg A, Eytan RI, Keck BP, Smith WL, Kuhn KL, Moore JA, Price SA, Burbrink FT, Friedman M, Wainwright PC (2013) Tempo of diversification in the superradiation of spiny-rayed fishes. Proc Natl Acad Sci 110:12738–12743

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nelson JS (2006) Fishes of the World. John Wiley and Sons, Hoboken, New Jersey

    Google Scholar 

  • Nielsen R (2002) Mapping mutations on phylogenies. Syst Biol 51:729–739

    Article  PubMed  Google Scholar 

  • Nunes F, Norris RD (2006) Abrupt reversal in ocean overturning during the Palaeocene/Eocene warm period. Nature 439:60–63

    Article  CAS  PubMed  Google Scholar 

  • O’Meara BC, Ane C, Sanderson MJ, Wainwright PC (2006) Testing for different rates of continuous trait evolution using likelihood. Evolution 60:922–933

    Article  PubMed  Google Scholar 

  • Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2013) caper: Comparative Analyses of Phylogenetics and Evolution in R. R package version 0.5.2. http://CRAN.R-project.org/package=caper

  • Pagel M (1997) Inferring evolutionary processes from phylogenies. Zool Scripta 26:331–348

    Article  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Perrin C (2002) Tertiary: the emergence of modern reef ecosystems. In: Kiessling W, Flugel E, Golonka J (eds) Phanerozoic reef patterns. SEPM (Society for Sedimentary Geology), Tulsa, pp 587–621

    Chapter  Google Scholar 

  • Price SA, Holzman RA, Near TJ, Wainwright PC (2011) Coral reefs promote the evolution of morphological diversity and ecological novelty in labrid fishes. Ecol Lett 14:462–469

    Article  CAS  PubMed  Google Scholar 

  • Price SA, Tavera J, Near TJ, Wainwright PC (2012) Elevated rates of morphological and functional diversification in reef-dwelling haemulid fishes. Evolution 67:417–428

    Article  PubMed  Google Scholar 

  • Price SA, Schmitz L, Oufiero C, Eytan RI, Dornburg A, Smith WL, Friedman M, Near TJ, Wainwright PC (2014) Two waves of colonization straddling the K–Pg boundary formed the modern reef fish fauna. Proc R Soc Lond B Biol Sci 281:20140321

    Article  CAS  Google Scholar 

  • R Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org

  • Rabosky D (2010) Primary controls on species richness in higher taxa. Syst Biol 59:634–645

    Article  PubMed  Google Scholar 

  • Rabosky D, Slater G, Alfaro M (2012) Clade age and species richness are decoupled across the eukaryotic tree of life. PLoS Biol 10:e1001381

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rabosky DL, Santini F, Eastman J, Smith SA, Sidlauskas B, Chang J, Alfaro ME (2013) Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nat Commun 4:1958

    Article  PubMed  Google Scholar 

  • Revell LJ (2011) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  • Ricklefs RE (2009) Speciation, extinction and diversity. In: Butlin RK, Bridle JR, Schluter D (eds) Speciation and patterns of diversity. Cambridge University Press, Cambridge, pp 257–277

    Chapter  Google Scholar 

  • Robertson DR (1998) Do coral-reef fish faunas have a distinctive taxonomic structure? Coral Reefs 17:179–186

    Article  Google Scholar 

  • Santini F, Tyler JC (2003) A phylogeny of the families of fossil and extant tetraodontiform fishes (Acanthomorpha, Tetraodontiformes), upper Cretaceous to recent. Zool J Linn Soc 139:565–617

    Article  Google Scholar 

  • Schoener TW (1974) Resource partitioning in ecological communities. Science 185

  • Smith WL, Craig MT (2007) Casting the percomorph net widely: the importance of broad taxonomic sampling in the search for the placement of serranid and percid fishes. Copeia 1:35–55

    Article  Google Scholar 

  • Stadler T, Rabosky DL, Ricklefs RE, Bokma F (2014) On age and species richness of higher taxa. Am Nat 184:447–455

    Article  PubMed  Google Scholar 

  • Vermeij GJ (1973a) Biological versatility and earth history. Proc Natl Acad Sci 70:1936–1938

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vermeij GJ (1973b) Adaptation, versatility, and evolution. Syst Zool 22:466–477

    Article  Google Scholar 

  • Zachos JC, Rohl U, Schellenberg SA, Sluijs A, Hodell DA, Kelly DC, Thomas E, Nicolo M, Raffi I, Lourens LJ, McCarren H, Kroon D (2005) Rapid acidification of the ocean during the Paleocene-Eocene thermal maximum. Science 308:1611–1615

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Jack Randall for making available his collection of photographs of Indo-Pacific fishes. This research was supported by NSF Grants IOS-0924489, DEB-1061981.

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Correspondence to S. A. Price.

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Communicated by Ecology Editor Dr. Alastair Harborne

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Price, S.A., Claverie, T., Near, T.J. et al. Phylogenetic insights into the history and diversification of fishes on reefs. Coral Reefs 34, 997–1009 (2015). https://doi.org/10.1007/s00338-015-1326-7

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  • DOI: https://doi.org/10.1007/s00338-015-1326-7

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