Macroevolutionary analysis of the tempo of diversification in snappers and fusiliers (Percomorpha: Lutjanidae)
DOI:
https://doi.org/10.26496/bjz.2017.2Keywords:
Lutjanus, phylogeny, ecological radiation, lineage diversification, molecular clockAbstract
The percomorph fish family Lutjanidae (snappers and fusiliers) includes about 135 reef-dwelling species, mainly confined to tropical and subtropical marine waters. The great majority of snappers are active predators feeding on fishes or crustaceans, even though some species, including the fusiliers (Caesioninae), have evolved zooplanktivory. Lutjanids show a great diversity of habitat preferences, based on depth segregation and distribution across reef and associated habitats (e.g., mangroves, seagrass beds, estuaries). In spite of their great ecological and economic importance little is known about the tempo of evolution in this group. The present study provides the most comprehensive molecular phylogeny to date for lutjanids, including 70% of extant species and 19 of the 21 currently described genera. We time-calibrated our molecular tree using the oldest described lutjanid fossils, and show how this group most likely originated during the Late Cretaceous or Early Paleocene. Lutjanids experienced a significant radiation during the Late Eocene and Early Oligocene, in contrast to a pattern of Late Oligocene/Miocene radiation observed in many other reef-associated groups. The time-tree allows us to investigate the tempo of diversification, and our results suggest a variation in the rate of speciation during the evolution of the major clade formed by “lutjanins and caesionins”. Variation in diet and life history strategies could explain this clade-specific dynamic, although future phylogenetic comparative studies combining additional ecological and morphological data are needed to test this hypothesis.References
Aburto-Oropeza O., Dominguez-Guerrero I., Cota-Nieto J. & Plomozo-Lugo T. (2009). Recruitment and ontogenetic habitat shifts of the yellow snapper (Lutjanus argentiventris) in the Gulf of California. Marine Biology 156: 2461–2472. https://doi.org/10.1007/s00227-009-1271-5
Alfaro M.E., Santini F. & Brock C.D. (2007). Do reefs drive diversification in marine teleosts? Evidence from the pufferfish and their allies (order Tetraodontiformes). Evolution 61: 2104–2126. https://doi.org/10.1111/j.1558-5646.2007.00182.x
Alfaro M.E., Brock C.D., Banbury B.L. & Wainwright P.C. (2009). Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes? BMC Evolutionary Biology 9: 255. https://doi.org/10.1186/1471-2148-9-255
Allen G.R. (1985). FAO species catalogue. Snappers of the world. An annotated and illustrated catalogue of lutjanid species known to date. FAO Fisheries Synopsis No. 125, Vol. 6, 208 pp.
Andrews K.R., Williams A.J., Fernandez-Silva I., Newman S.J., Copus J.M., Wakefield C.B., Randall J.E. & Bowen B.W. (2016). Phylogeny of deepwater snappers (Genus Etelis) reveals a cryptic species pair in the Indo-Pacific and Pleistocene invasion of the Atlantic. Molecular Phylogenetics and Evolution 100: 361–371. https://doi.org/10.1016/j.ympev.2016.04.004
Bannikov A.F. (2006). Fishes from the Eocene of Bolca, northern Italy, previously classified in the Sparidae, Serranidae and Haemulidae (Perciformes). Geodiversitas 28 (2): 249–275.
Bellwood D.R., Goatley C.H.R. & Bellwood O. (2016). The evolution of fishes and corals on reefs: form, function and interdependence. Biological Reviews 92 (2): 878–901. https://doi.org/10.1111/brv.12259
Berkström C., Jörgensen T. & Hellström M. (2013). Ecological connectivity and niche differentiation between two closely related fish species in the mangrove−seagrass−coral reef continuum. Marine Ecology Progress Series 477: 201–215. https://doi.org/10.3354/meps10171
Betancur-R. R., Broughton R.E., Wiley E.O., Carpenter K., López J.A., Li C., Holcroft N.I., Arcila D., Sanciangco M., Cureton II J.C., Zhang F., Buser T., Campbell M.A., Ballesteros J.A., Roa-Varon A., Willis S., Borden W.C., Rowley T., Reneau P.C., Hough D.J., Lu G., Grande T., Arratia G. & Ortí G. (2013). The Tree of Life and a new classification of bony fishes. PLoS Currents Tree of Life. Edition 1, 18 April 2013. https://doi.org/10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288
Blot J. & Tyler J.C. (1990). New genera and species of fossil surgeonfishes and their relatives (Acanthuroidei, Teleostei) from the Eocene of Monte Bolca, Italy, with application of the Blot formula to both fossil and recent forms. Studi e Ricerche sui Giacimenti Terziari di Bolca 6: 13–92.
Briggs J.C. & Bowen B.W. (2012). A realignment of marine biogeographic provinces with particular reference to fish distributions. Journal of Biogeography 39: 12–30. https://doi.org/10.1111/j.1365-2699.2011.02613.x
Burnham K.P. & Anderson D.R. (2002). Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York.
Carnevale G., Bannikov A.F., Marramà G., Tyler J.C. & Zorzin R. (2014). The Pesciara-Monte Postale Fossil-Lagerstätte: fishes and other vertebrates. Rendiconti della Società Paleontologica Italiana 4: 37–63.
Chen W.-J., Santini F., Carnevale G., Chen J.-N., Liu S.-H., Lavoué S. & Mayden R.L. (2014). New insights on early evolution of spiny-rayed fishes (Teleostei: Acanthomorpha). Frontiers in Marine Sciences 53: 1. https://doi.org/10.3389/fmars.2014.00053
Chu C., Rizman-Idid M. & Ching C.V. (2013). Phylogenetic relationships of selected genera of Lutjanidae inferred from mitochondrial regions, with a note on the taxonomic status of Pinjalo pinjalo. Ciencias Marinas 39 (4): 349–361. https://doi.org/10.7773/cm.v39i4.2287
Cocheret de la Morinière E., Pollux B.J.A., Nagelkerken I., Hemminga M.A., Huiskes A.H.L. & Van der Velde G. (2003). Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: Stable isotopes and gut-content analysis. Marine Ecology Progress Series 246: 279–289. https://doi.org/10.3354/meps246279
Cooper W.J & Santini F. (2016). A revised damselfish taxonomy with a description of the tribe Microspathodontini (giant damselfishes). In: Frédérich B. & Parmentier E. (eds) Biology of Damselfishes: 15–30. CRC Press, Boca Raton.
Cowman P.F. & Bellwood D.R. (2011). Coral reefs as drivers of cladogenesis: Expanding coral reefs, cryptic extinction events, and the development of biodiversity hotspots. Journal of Evolutionary Biology 24: 2543–2562. https://doi.org/10.1111/j.1420-9101.2011.02391.x
Dornburg A., Sidlauskas B., Santini F., Sorenson L., Near T.J. & Alfaro M.E. (2011). The influence of an innovative locomotor strategy on the phenotypic diversification of triggerfish (family: Balistidae). Evolution 65: 1912–1926. https://doi.org/10.1111/j.1558-5646.2011.01275.x
Drummond A.J. & Rambaut A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214. https://doi.org/10.1186/1471-2148-7-214
Edgar R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797. https://doi.org/10.1093/nar/gkh340
Eschmeyer W.N., Fricke R. & van der Laan R. (2016). Catalog of Fishes. Available from http://www.calacademy.org/scientists/projects/catalog-of-fishes [accessed 31 Aug. 2016].
Frédérich B., Sorenson L., Santini F., Slater G.J. & Alfaro M.E. (2013). Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae). The American Naturalist 181: 94–113. https://doi.org/10.1086/668599
Froese R. & Pauly D. (2016). FishBase. Available from www.fishbase.org [accessed 30 Sep. 2016].
Gold J.R., Voelker G. & Renshaw M.A. (2011). Phylogenetic relationships of tropical western Atlantic snappers in subfamily Lutjaninae (Lutjanidae: Perciformes) inferred from mitochondrial DNA sequences. Biological Journal of the Linnean Society 102: 915–929. https://doi.org/10.1111/j.1095-8312.2011.01621.x
Gold J.R., Willis S.C., Renshaw M.A., Buentello A., Walker Jr. H.J., Puritz J.B., Hollenbeck C.M. & Voelker G. (2015). Phylogenetic relationships of tropical eastern Pacific snappers (Lutjanidae) inferred from mitochondrial DNA sequences. Systematics and Biodiversity 13 (6): 596–607. https://doi.org/10.1080/14772000.2015.1078857
Iwatsuki Y., Tanaka F. & Allen G.R. (2015). Lutjanus xanthopinnis, a new species of snapper (Pisces: Lutjanidae) from the Indo-west Pacific, with a redescription of Lutjanus madras (Valenciennes 1831). Journal of the Ocean Science Foundation 17: 22–42.
Johnson G.D. (1980). The limits and relationships of the Lutjanidae and associated families. Bulletin of the Scripps Institution of Oceanography 24: 1–114.
Johnson G.D. (1993). Percomorph phylogeny: progress and problems. Bulletin of Marine Science 52: 3–28.
Kazancioglu E., Near T.J., Hanel R. & Wainwright P.C. (2009). Influence of sexual selection and feeding functional morphology on diversification rate of parrotfishes (Scaridae). Proceedings of the Royal Society B-Biological Sciences 276: 3439–3446. https://doi.org/10.1098/rspb.2009.0876
Lanfear R., Calcott B., Ho S.Y.W. & Guindon S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29: 1695–1701. https://doi.org/10.1093/molbev/mss020
Litsios G., Pearman P.B., Lanterbecq D., Tolou N. & Salamin N. (2014). The radiation of the clownfishes has two geographical replicates. Journal of Biogeography 41: 2140–2149. https://doi.org/10.1111/jbi.12370
Lobato F.L., Barneche D.R., Siqueira A.C., Liedke A.M.R., Lindner A., Pie M.R., Bellwood D.R. & Floeter S.R. (2014). Diet and diversification in the evolution of coral reef fishes. PLoS ONE 9 (7): e102094. https://doi.org/10.1371/journal.pone.0102094
Lythgoe J.N., Muntz W.R.A., Partridge J.C., Shand J. & Williams D.M. (1994). The ecology of the visual pigments of snappers (Lutjanidae) on the Great Barrier Reef. Journal of Comparative Physiology A 174: 461–467. https://doi.org/10.1007/BF00191712
Maddison W.P. & Maddison D.R. (2015). Mesquite: a modular system for evolutionary analysis, version 3.01. Available from http://www.mesquiteproject.org [accessed 24 Apr. 2017].
Martinez-Andrade F. (2003) A comparison of life histories and ecological aspects among snappers (PISCES: Lutjanidae). Louisiana State University, Department of Oceanography and Coastal Sciences, PhD Thesis, 194 pp.
Miller T.L. & Cribb T.H. (2007). Phylogenetic relationships of some common Indo-Pacific snappers (Perciformes: Lutjanidae) based on mitochondrial DNA sequences, with comments on the taxonomic position of the Caesioninae. Molecular Phylogenetics and Evolution 44: 450–460. https://doi.org/10.1016/j.ympev.2006.10.029
Monteiro D.P., Giarrizzo T. & Isaac V. (2009). Feeding ecology of juvenile dog snapper Lutjanus jocu (Bloch and Shneider, 1801) (Lutjanidae) in intertidal mangrove creeks in Curuçá estuary (Northern Brazil). Brazilian Archives of Biology and Technology 52: 1421–1430. https://doi.org/10.1590/S1516-89132009000600014
Nagelkerken I., van der Velde G., Gorissen M.W., Meijer G.J., van’t Hof T. & den Hartog C. (2000). Importance of mangroves, seagrass beds and the shallow coral reef as a nursery for important coral reef fishes, using a visual census technique. Estuarine, Coastal and Shelf Science 51: 31–44. https://doi.org/10.1006/ecss.2000.0617
Near T.J., Dornburg A., Eytan R.I., Keck B., Smith W.L., Kuhn K.L., Moore J.A., Price S.A., Burbrink F.T., Friedman M. & Wainwright P.C. (2013). Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes. Proceedings of the National Academy of Sciences of the United States of America 110: 12738–12743. https://doi.org/10.1073/pnas.1304661110
Newman S.J. (1995). Spatial variability in the distribution, abundance, growth, mortality and age structures of tropical snappers (Pisces: Lutjanidae) in the Central Great Barrier Reef, Australia. James Cook University, Department of Marine Biology, PhD Thesis, 325 pp.
Newman S.J. & Williams D.M. (1996). Variation in reef associated assemblages of the Lutjanidae and Lethrinidae at different distances offshore in the central Great Barrier Reef. Environmental Biology of Fishes 46: 123–138. https://doi.org/10.1007/BF00005214
Pimentel C.R. & Joyeux J.-C. (2010). Diet and food partitioning between juveniles of mutton Lutjanus analis, dog Lutjanus jocu and lane Lutjanus synagris snappers (Perciformes: Lutjanidae) in a mangrove-fringed estuarine environment. Journal of Fish Biology 76: 2299–2317. https://doi.org/10.1111/j.1095-8649.2010.02586.x
Pybus O.G. & Harvey P.H. (2000). Testing macro-evolutionary models using incomplete molecular phylogenies. Proceedings of the Royal Society, Series B-Biological Sciences 267: 2267–2272. https://doi.org/10.1098/rspb.2000.1278
Rabosky D.L. (2006). LASER: a maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Evolutionary Bioinformatics 2: 247–250.
Rabosky D.L. & Lovette I.J. (2008). Density-dependent diversification in North American wood warblers. Proceedings of the Royal Society Series B-Biological Sciences 275: 2363–2371. https://doi.org/10.1098/rspb.2008.0630
Rabosky D.L., Santini F., Eastman J., Smith S.A., Sidlauskas B., Chang J. & Alfaro M.E. (2013). Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nature Communications 4: 1958. https://doi.org/10.1038/ncomms2958
R Development Core Team (2015). R: A language and environment for statistical computing. Vienna, Austria. Available from http://www.R-project.org [accessed 25 Aprl. 2017].
Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. (2012). MrBayes 3.2: Efficient bayesian phylogenetic inference and model Choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
Sanderson M.J., Boss D., Chen D., Cranston K.A. & Wehe A. (2008). The PhyLoTA Browser: processing GenBank for molecular phylogenetics research. Systematic Biology 57: 335–346. https://doi.org/10.1080/10635150802158688
Santini F. & Tyler J.C. (2003). A phylogeny of the families of fossil and extant tetraodontiform fishes (Acanthomorpha, Tetraodontiformes), Upper Cretaceous to recent. Zoological Journal of the Linnean Society 139: 565–617. https://doi.org/10.1111/j.1096-3642.2003.00088.x
Santini F. & Winterbottom R. (2002). Historical biogeography of Indo-western Pacific coral reef biota: is the Indonesian region a centre of origin? Journal of Biogeography 29: 189–205. https://doi.org/10.1046/j.1365-2699.2002.00669.x
Santini F., Nguyen M., Sorenson M., Waltzek T.B., Alfaro J.W.L., Eastman J.M. & Alfaro M.E. (2013a). Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae). Journal of Evolutionary Biology 26: 1003–1018. https://doi.org/10.1111/jeb.12112
Santini F., Sorenson L. & Alfaro M.E. (2013b). A new multi-locus timescale reveals the evolutionary basis of diversity patterns in triggerfishes and filefishes (Balistidae, Monacanthidae; Tetraodontiformes). Molecular Phylogenetics and Evolution 69:165–176. https://doi.org/10.1016/j.ympev.2013.05.015
Santini F., Carnevale G. & Sorenson L. (2014). First multi-locus timetree of seabreams and porgies (Percomorpha: Sparidae). Italian Journal of Zoology 81: 55–71. https://doi.org/10.1080/11250003.2013.878960
Sarver S.K., Freshwater D.W. & Walsh P. (1996). Phylogenetic relationships of western Atlantic snappers (family Lutjanidae) based on mitochondrial DNA sequences. Copeia 1996: 715–721.
Streelman J.T., Alfaro M.E., Westneat M.W., Bellwood D.R. & Karl S.A. (2002). Evolutionary history of the parrotfishes: biogeography, ecomorphology, and comparative diversity. Evolution 56: 961–971. https://doi.org/10.1111/j.0014-3820.2002.tb01408.x
Swift C. & Ellwood B. (1972). Hypsocephalus atlanticus, a new genus and species of lutjanid fish from marine Eocene limestones of Northern Florida. Contributions in Science 230: 1–29.
Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729. https://doi.org/10.1093/molbev/mst197
Tyler J.C. (1999). A new genus and species of surgeonfish (Acanthuridae) with a unique dorsal-fin pterygiophore arrangement from the Eocene of Monte Bolca, Italy. Studi e Ricerche sui Giacimenti Terziari di Bolca 7: 245–256.
Tyler J.C. (2005a). Redescription and basal phylogenetic placement of the acanthurid surgeonfish Gazolaichthys vestenanovae from the Eocene of Monte Bolca, Italy (Perciformes; Acanthuroidea). Studi e Ricerche sui Giacimenti Terziari di Bolca 11: 97–117.
Tyler J.C. (2005b). A new genus for the surgeon fish Acanthurus gaudryi De Zigno 1887 from the Eocene of Monte Bolca, Italy, amorphologically primitive basal taxon of Acanthuridae (Acanthuroidea, Perciformes). Studi e Ricerche sui Giacimenti Terziari di Bolca 11: 149–163.
Tyler J.C. & Bannikov A.F. (2000). A new species of the surgeon fish genus Tauichthys from the Eocene of Monte Bolca, Italy (Perciformes, Acanthuridae). Bollettino del Museo Civico di Storia Naturale di Verona 24: 29–36.
Tyler J.C. & Santini F. (2002). Review and reconstructions of the tetraodontiform fishes from the Eocene of Monte Bolca, Italy, with comments on related Tertiary taxa. Studi e Ricerche sui Giacimenti Terziari di Bolca 9: 47–119.
Wakefield C.B., Moore G.I., Bertram A.E., Snow M. & Newman S.J. (2016). Extraordinary capture of a Randall’s snapper Randallichthys filamentosus in the temperate south-eastern Indian Ocean and its molecular phylogenetic relationship within the Etelinae. Journal of Fish Biology 88: 735–740. https://doi.org/10.1111/jfb.12809
Yang Z. (2006). Computational Molecular Evolution. Oxford University Press, Oxford.
Zhou F., Jiang S., Su T. & Lu J. (2004). Comparative study of mtDNA 16S rRNA gene fragments among six Lutjanus fish. Journal of Fisheries Science 11: 99–103.
Zhu S.-H., Yang Y.-C., Shen X.-Q., Zou J.-X., Zheng W.-J., Yu H.-W. & Huang B. (2006). Phylogenetic relationships of Lutjanus inferred from mitochondrial cytochrome b sequences. Acta Zoologica Sinica 52: 514–521.
Downloads
Published
How to Cite
Issue
Section
License
All published papers will be put on-line as high resolution PDF’s. Copyright thus remains with the authors. All manuscripts will be licensed under a Creative Commons Attribution 3.0 License https://creativecommons.org/licenses/by/4.0/.
