OpenLB
Open Library of Bioscience
Advanced Search
Scientific reports
10 20, 2021;11 (1): 20731.

Influence of historical changes in tropical reef habitat on the diversification of coral reef fishes.

Fabien Leprieur, Loic Pellissier, David Mouillot, Théo Gaboriau
Author Information
  1. Fabien Leprieur: UMR MARBEC (CNRS, IRD, IFREMER, UM), Université de Montpellier, Place Eugène Bataillon, 34095, Montpellier Cedex 5, France.
  2. Loic Pellissier: Landscape Ecology, Institute of Terrestrial Ecosystems, ETH Zürich, 8092, Zurich, Switzerland.
  3. David Mouillot: UMR MARBEC (CNRS, IRD, IFREMER, UM), Université de Montpellier, Place Eugène Bataillon, 34095, Montpellier Cedex 5, France.
  4. Théo Gaboriau: Department of Computational Biology, University of Lausanne, 1015, Lausanne, Switzerland. theo.gaboriau@unil.ch.
PMID: 34671048 DOI: 10.1038/s41598-021-00049-4

Abstract

Past environmental changes are expected to have profoundly impacted diversity dynamics through time. While some previous studies showed an association between past climate changes or tectonic events and important shifts in lineage diversification, it is only recently that past environmental changes have been explicitly integrated in diversification models to test their influence on diversification rates. Here, we used a global reconstruction of tropical reef habitat dynamics during the Cenozoic and phylogenetic diversification models to test the influence of (i) major geological events, (ii) reef habitat fragmentation and (iii) reef area on the diversification of 9 major clades of tropical reef fish (Acanthuridae, Balistoidea, Carangoidea, Chaetodontidae, Haemulinae, Holocentridae, Labridae, Pomacentridae and Sparidae). The diversification models revealed a weak association between paleo-habitat changes and diversification dynamics. Specifically, the fragmentation of tropical reef habitats over the Cenozoic was found to be a driver of tropical reef fish diversification for 2 clades. However, overall, our approach did not allow the identification of striking associations between diversification dynamics and paleo-habitat fragmentation in contrast with theoretical model's predictions.

References

  1. Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived?. Nature 471, 51–57 (2011). [PMID: 21368823]
  2. Zaffos, A., Finnegan, S. & Peters, S. E. Plate tectonic regulation of global marine animal diversity. Proc. Natl. Acad. Sci. 114, 5653–5658 (2017). [PMID: 28507147]
  3. Claramunt, S. & Cracraft, J. A new time tree reveals Earth historys imprint on the evolution of modern birds. Sci. Adv. 1, e1501005 (2015). [PMID: 26824065]
  4. Leprieur, F., Descombes, P., Gaboriau, T., Cowman, P. F. & Parravicini, V. Plate tectonics drive tropical reef biodiversity dynamics. Nat. Commun. 7, 11461 (2016). [PMID: 27151103]
  5. Ficetola, G. F., Mazel, F. & Thuiller, W. Global determinants of zoogeographical boundaries. Nat. Ecol. Evol. 1, 0089 (2017). [DOI: 10.1038/s41559-017-0089]
  6. Mazel, F. et al. Global patterns of β-diversity along the phylogenetic time-scale: The role of climate and plate tectonics. Glob. Ecol. Biogeogr. 26, 1211–1221 (2017). [DOI: 10.1111/geb.12632]
  7. Hofreiter, M. & Stewart, J. Ecological change, range fluctuations and population dynamics during the pleistocene. Curr. Biol. 19, R584–R594 (2009). [PMID: 19640497]
  8. Pellissier, L. et al. Quaternary coral reef refugia preserved fish diversity. Science 344, 1016–1019 (2014). [PMID: 24876495]
  9. Jaramillo, C. et al. Effects of rapid global warming at the paleocene-eocene boundary on neotropical vegetation. Science 330, 957–961 (2010). [PMID: 21071667]
  10. Svenning, J.-C., Eiserhardt, W. L., Normand, S., Ordonez, A. & Sandel, B. The influence of paleoclimate on present-day patterns in biodiversity and ecosystems. Annu. Rev. Ecol. Evol. Syst. 46, 551–572 (2015). [DOI: 10.1146/annurev-ecolsys-112414-054314]
  11. Steeman, M. E. et al. Radiation of extant cetaceans driven by restructuring of the oceans. Syst. Biol. 58, 573–585 (2009). [PMID: 20525610]
  12. Antonelli, A. & Sanmartín, I. Mass Extinction, gradual cooling, or rapid radiation? reconstructing the spatiotemporal evolution of the ancient angiosperm genus hedyosmum (Chloranthaceae) using empirical and simulated approaches. Syst. Biol. 60, 596–615 (2011). [PMID: 21856636]
  13. Nee, S., May, R. M. & Harvey, P. H. The reconstructed evolutionary process. Philos. Trans. R. Soc. Lond. B 344, 305–311 (1994). [DOI: 10.1098/rstb.1994.0068]
  14. Morlon, H., Parsons, T. L. & Plotkin, J. B. From the cover: Reconciling molecular phylogenies with the fossil record. Proc. Natl. Acad. Sci. 108, 16327–16332 (2011). [PMID: 21930899]
  15. Condamine, F. L., Rolland, J. & Morlon, H. Macroevolutionary perspectives to environmental change. Ecol. Lett. 16, 72–85 (2013). [PMID: 23331627]
  16. Condamine, F. L. et al. Deciphering the evolution of birdwing butterflies 150 years after Alfred Russel Wallace Deciphering the evolution of birdwing butterflies 150 years after. Sci. Rep. 5, 11860 (2015). [PMID: 26133078]
  17. Lagomarsino, L. P., Condamine, F. L., Antonelli, A., Mulch, A. & Davis, C. C. The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytol. 210, 1430–1442 (2016). [PMID: 26990796]
  18. Rolland, J. & Condamine, F. L. The contribution of temperature and continental fragmentation to amphibian diversification. J. Biogeogr. 46, 1857–1873 (2019). [DOI: 10.1111/jbi.13592]
  19. Gaboriau, T. et al. Ecological constraints coupled with deep-time habitat dynamics predict the latitudinal diversity gradient in reef fishes. Proc. R. Soc. B Biol. Sci. 286, 20191506 (2019). [DOI: 10.1098/rspb.2019.1506]
  20. Descombes, P. et al. Linking species diversification to palaeo-environmental changes: A process-based modelling approach. Glob. Ecol. Biogeogr. 00, 1–12 (2017).
  21. Rangel, T. F. et al. Modeling the ecology and evolution of biodiversity: Biogeographical cradles, museums, and graves. Science 361, 5452 (2018). [DOI: 10.1126/science.aar5452]
  22. Pontarp, M. et al. The latitudinal diversity gradient: Novel understanding through mechanistic eco-evolutionary models. Trends Ecol. Evol. 34, 211–223 (2019). [PMID: 30591209]
  23. Cowman, P. F. Historical factors that have shaped the evolution of tropical reef fishes: A review of phylogenies, biogeography, and remaining questions. Front. Genet. 5, 1–15 (2014). [DOI: 10.3389/fgene.2014.00394]
  24. Bellwood, D. R. et al. Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes. J. Evol. Biol. 23, 335–349 (2010). [PMID: 20487131]
  25. Cowman, P. F. & Bellwood, D. R. Coral reefs as drivers of cladogenesis: Expanding coral reefs, cryptic extinction events, and the development of biodiversity hotspots. J. Evol. Biol. 24, 2543–2562 (2011). [PMID: 21985176]
  26. Sorenson, L., Santini, F., Carnevale, G. & Alfaro, M. E. A multi-locus timetree of surgeonfishes (Acanthuridae, Percomorpha), with revised family taxonomy. Mol. Phylogenet. Evol. 68, 150–160 (2013). [PMID: 23542000]
  27. Dornburg, A., Moore, J., Beaulieu, J. M., Eytan, R. I. & Near, T. J. The impact of shifts in marine biodiversity hotspots on patterns of range evolution: Evidence from the Holocentridae (squirrelfishes and soldierfishes). Evolution 69, 146–161 (2015). [PMID: 25407924]
  28. Cowman, P. F. & Bellwood, D. R. The historical biogeography of coral reef fishes: Global patterns of origination and dispersal. J. Biogeogr. 40, 209–224 (2013). [DOI: 10.1111/jbi.12003]
  29. Lohman, D. J. et al. Biogeography of the Indo-Australian archipelago. Annu. Rev. Ecol. Evol. Syst. 42, 205–226 (2011). [DOI: 10.1146/annurev-ecolsys-102710-145001]
  30. Gaboriau, T., Leprieur, F., Mouillot, D. & Hubert, N. Influence of the geography of speciation on current patterns of coral reef fish biodiversity across the Indo-Pacific. Ecography 41, 1295–1306 (2017). [DOI: 10.1111/ecog.02589]
  31. McManus, J. W. Marine speciation, tectonics and sea- level changes in Southeast Asia. Proc. Fifth Int. Coral Reef 4, 133–138 (1985).
  32. Potts, D. C. Sea-level fluctuations and speciation in Scleractinia. Proc. Fifth Int. Coral Reef 4, 51–62 (1985).
  33. Hou, Z. & Li, S. Tethyan changes shaped aquatic diversification. Biol. Rev. https://doi.org/10.1111/brv.12376 (2017). [DOI: 10.1111/brv.12376]
  34. Stadler, T. Mammalian phylogeny reveals recent diversification rate shifts. Proc. Natl. Acad. Sci. USA 108, 6187–6192 (2011). [PMID: 21444816]
  35. Bellwood, D. R. & Wainwright, P. C. The history and biogeography of Fishes on Coral Reefs. in Coral Reef Fishes, Dynamics and Diversity in a Complex Ecosystem, 5–32 (2002).
  36. Williams, S. T. & Duda, T. F. Did tectonic activity stimulate Oligo-Miocene speciation in the Indo-West Pacific?. Evolution 62, 1618–1634 (2008). [PMID: 18410535]
  37. Renema, W. et al. Hopping hotspots: Global shifts in marine biodiversity. Science 321, 654–657 (2008). [PMID: 18669854]
  38. Tea, Y.-K. et al. Phylogenomic analysis of concatenated ultraconserved elements reveals the recent evolutionary radiation of the fairy wrasses (teleostei: labridae: cirrhilabrus). Syst. Biol. 1, 1–12 (2021). [DOI: 10.1093/sysbio/syab012]
  39. Hall, R. Southeast Asia’s changing palaeogeography. Blumea J. Plant Taxon. Plant Geogr. 54, 148–161 (2009). [DOI: 10.3767/000651909X475941]
  40. Keith, S. A., Baird, A. H., Hughes, T. P., Madin, J. S. & Connolly, S. R. Faunal breaks and species composition of Indo-Pacific corals: The role of plate tectonics, environment and habitat distribution. Proc. Biol. Sci. 280, 20130818 (2013). [PMID: 23698011]
  41. Cowman, P. F. & Bellwood, D. R. Vicariance across major marine biogeographic barriers: Temporal concordance and the relative intensity of hard versus soft barriers. Proc. Biol. Sci. 280, 20131541 (2013). [PMID: 23945690]
  42. Price, S. A., Claverie, T., Near, T. J. & Wainwright, P. C. Phylogenetic insights into the history and diversification of fishes on reefs. Coral Reefs 34, 997–1009 (2015). [DOI: 10.1007/s00338-015-1326-7]
  43. Bellwood, D. R., Goatley, C. H. R. & Bellwood, O. The evolution of fishes and corals on reefs: Form, function and interdependence. Biol. Rev. 92, 878–901 (2017). [PMID: 26970292]
  44. Bowen, B. W., Rocha, L. A., Toonen, R. J. & Karl, S. A. The origins of tropical marine biodiversity. Trends Ecol. Evol. 28, 359–366 (2013). [PMID: 23453048]
  45. Price, S. A., Tavera, J. J., Near, T. J. & Wainwright, P. C. Elevated rates of morphological and functional diversification in reef-dwelling haemulid fishes. Evolution 67, 417–428 (2012). [PMID: 23356614]
  46. Kiessling, W., Simpson, C., Beck, B., Mewis, H. & Pandolfi, J. M. Equatorial decline of reef corals during the last Pleistocene interglacial. Proc. Natl. Acad. Sci. USA. 109, 21378–21383 (2012). [PMID: 23236154]
  47. Floeter, S. R. et al. Atlantic reef fish biogeography and evolution. J. Biogeogr. 35, 22–45 (2007).
  48. Riginos, C., Buckley, Y. M., Blomberg, S. P. & Treml, E. A. Dispersal capacity predicts both population genetic structure and species richness in reef fishes. Am. Nat. 184, 52–64 (2014). [PMID: 24921600]
  49. Rocha, L. A. & Bowen, B. W. Speciation in coral-reef fishes. J. Fish Biol. 72, 1101–1121 (2008). [DOI: 10.1111/j.1095-8649.2007.01770.x]
  50. Tedesco, P. A., Paradis, E., EvEque, C. L. & Hugueny, B. Explaining global-scale diversification patterns in actinopterygian fishes. J. Biogeogr. 44, 773–783 (2016). [DOI: 10.1111/jbi.12905]
  51. Rosenzweig, M. L. Species Diversity in Space and Time (Springer, 1995). [DOI: 10.1017/CBO9780511623387]
  52. Kisel, Y. & Barraclough, T. G. Speciation has a spatial scale that depends on levels of gene flow. Am. Nat. 175, 316–334 (2010). [PMID: 20100106]
  53. Fine, P. V. A. & Ree, R. H. Evidence for a time-integrated species-area effect on the latitudinal gradient in tree diversity. Am. Nat. 168, 796–804 (2006). [PMID: 17109321]
  54. Jetz, W. & Fine, P. V. A. Global gradients in vertebrate diversity predicted by historical area-productivity dynamics and contemporary environment. PLoS Biol. 10, e1001292 (2012). [PMID: 22479151]
  55. Konow, N., Price, S., Abom, R., Bellwood, D. & Wainwright, P. Decoupled diversification dynamics of feeding morphology following a major functional innovation in marine butterflyfishes. Proc. Biol. Sci. 284, 20170906 (2017). [PMID: 28768889]
  56. Clements, K. D., German, D. P., Piché, J., Tribollet, A. & Choat, J. H. Integrating ecological roles and trophic diversification on coral reefs: Multiple lines of evidence identify parrotfishes as microphages. Biol. J. Linn. Soc. 120, 729–751 (2017).
  57. Lobato, F. L. et al. Diet and diversification in the evolution of coral reef fishes. PLoS ONE 9, e102094 (2014). [PMID: 25029229]
  58. Siqueira, A. C., Morais, R. A., Bellwood, D. R. & Cowman, P. F. Trophic innovations fuel reef fish diversification. Nat. Commun. 11, 1–11 (2020). [DOI: 10.1038/s41467-020-16498-w]
  59. Louca, S. & Pennell, M. W. Extant timetrees are consistent with a myriad of diversification histories. Nature 580, 502–505 (2020). [PMID: 32322065]
  60. Morlon, H., Hartig, F. & Robin, S. Prior hypotheses or regularization allow inference of diversification histories from extant timetrees. bioRxiv (2020).
  61. McCord, C. L. & Westneat, M. W. Phylogenetic relationships and the evolution of BMP4 in triggerfishes and filefishes (Balistoidea). Mol. Phylogenet. Evol. 94, 397–409 (2016). [PMID: 26408967]
  62. Santini, F. & Carnevale, G. First multilocus and densely sampled timetree of trevallies, pompanos and allies (Carangoidei, Percomorpha) suggests a Cretaceous origin and Eocene radiation of a major clade of piscivores. Mol. Phylogenet. Evol. 83, 33–39 (2015). [PMID: 25450104]
  63. Santini, F., Carnevale, G. & Sorenson, L. First multi-locus timetree of seabreams and porgies (Percomorpha: Sparidae). Ital. J. Zool. 81, 55–71 (2014). [DOI: 10.1080/11250003.2013.878960]
  64. Müller, R. D., Sdrolias, M., Gaina, C., Steinberger, B. & Heine, C. Long-term sea-level fluctuations driven by ocean basin dynamics. Science 319, 1357–1362 (2008). [PMID: 18323446]
  65. Heine, C., Yeo, L. G. & Müller, R. D. Evaluating global paleoshoreline models for the Cretaceous and Cenozoic. Aust. J. Earth Sci. 62, 275–287 (2015).
  66. Kleypas, J. A. & Mcmanus, J. W. Environmental Limits to Coral Reef Development : Where Do We Draw the Line ?. Am. Zool. 39, 146–159 (1999). [DOI: 10.1093/icb/39.1.146]
  67. Bugayevskiy, L. M. & Snyder, J. P. Map Projections: A Reference Manual (Taylor & Francis, London, 1995).
  68. Chang, J., Rabosky, D. L. & Alfaro, M. E. Estimating diversification rates on incompletely sampled phylogenies: Theoretical concerns and practical solutions. Syst. Biol. 69, 602–611 (2020). [PMID: 31804691]
  69. Morlon, H. et al. RPANDA: An R package for macroevolutionary analyses on phylogenetic trees. Methods Ecol. Evol. 7, 589–597 (2016). [DOI: 10.1111/2041-210X.12526]

MeSH Term

Animals
Biodiversity
Climate Change
Coral Reefs
Ecosystem
Fishes
Geology
Phylogeny
Journal Article
Article has an altmetric score of 1

Word Cloud

Created with Highcharts 10.0.0diversificationreefchangestropicaldynamicsmodelshabitatfragmentationenvironmentalassociationpasteventstestinfluenceCenozoicmajorcladesfishpaleo-habitatPastexpectedprofoundlyimpacteddiversitytimepreviousstudiesshowedclimatetectonicimportantshiftslineagerecentlyexplicitlyintegratedratesusedglobalreconstructionphylogeneticgeologicaliiiiiarea9AcanthuridaeBalistoideaCarangoideaChaetodontidaeHaemulinaeHolocentridaeLabridaePomacentridaeSparidaerevealedweakSpecificallyhabitatsfounddriver2Howeveroverallapproachallowidentificationstrikingassociationscontrasttheoreticalmodel'spredictionsInfluencehistoricalcoralfishes

Similar Articles

Cited By