[en] Various factors may impact the processes of diversification of a clade. In the marine realm, it has been shown that coral reef environments have promoted diversification in various fish groups. With the exception of requiem sharks, all the groups showing a higher level of diversity in reefs than in non-reef habitats have diets based predominantly on plankton, algae or benthic invert- ebrates. Here we explore the pattern of diversification of carangoid fishes, a clade that includes numerous piscivorous species (e.g. trevallies, jacks and dolphinfishes), using time-calibrated phylogenies as well as ecological and morphological data from both extant and fossil species. The study of caran- goid morphospace suggests that reef environments played a role in their early radiation during the Eocene. However, contrary to the hypothesis of a reef-association-promoting effect, we show that habitat shifts to non-reef environments have increased the rates of morphological diversification (i.e. size and body shape) in extant carangoids. Piscivory did not have a major impact on the tempo of diversification of this group. Through the ecological radiation of carangoid fishes, we demonstrate that non-reef environments may sustain and promote processes of diversification of different marine fish groups, at least those including a large proportion of piscivorous species.
Research center :
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
Disciplines :
Zoology
Author, co-author :
Frederich, Bruno ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Marrama, Giuseppe
Carnevale, Giorgio
Santini, Francesco
Language :
English
Title :
Non-reef environments impact the diversification of extant jacks, remoras and allies (Carangoidei, Percomorpha)
Publication date :
02 November 2016
Journal title :
Proceedings of the Royal Society. Biological Sciences
ISSN :
0962-8452
eISSN :
1471-2954
Publisher :
Royal Society, London, United Kingdom
Volume :
283
Pages :
20161556
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Albert AYK, Sawaya S, Vines TH, Knecht AK, Miller CT, Summers BR, Balabhadra S, Kingsley DM, Schluter D. 2008 The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution 62, 76-85. (doi:10.1111/j.1558-5646. 2007.00259.x)
Rojas D, Vale A, Ferrero V, Navarro L. 2012 The role of frugivory in the diversification of bats in the Neotropics. J. Biogeogr. 39, 1948-1960. (doi:10. 1111/j.1365-2699.2012.02709.x)
Price SA, Wainwright PC, Bellwood DR, Kazancioglu E, Collar DC, Near TJ. 2010 Functional innovations and morphological diversification in parrotfish. Evolution 64, 3057-3068. (doi:10.1111/j.1558-5646.2010.01036.x)
Dornburg A, Sidlauskas B, Santini F, Sorenson L, Near TJ, Alfaro ME. 2011 The influence of an innovative locomotor strategy on the phenotypic diversification of triggerfish (family: Balistidae). Evolution 65, 1912-1926. (doi:10.1111/j.1558-5646.2011.01275.x)
Higham TE, Birn-Jeffery AV, Collins CE, Hulsey CD, Russell AP. 2015 Adaptive simplification and the evolution of gecko locomotion: morphological and biomechanical consequences of losing adhesion. Proc. Natl Acad. Sci. USA 112, 809-814. (doi:10.1073/pnas.1418979112)
Arbuckle K, Speed MP. 2015 Antipredator defenses predict diversification rates. Proc. Natl Acad. Sci. USA 112, 13597-13602. (doi:10.1073/pnas.150981 1112)
Schluter D. 2000 The ecology of adaptive radiation. Oxford, UK: Oxford University Press.
Alfaro ME, 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. (doi:10.1111/j.1558-5646.2007.00182.x)
Price SA, Holzman R, Near TJ, Wainwright PC. 2011 Coral reefs promote the evolution of morphological diversity and ecological novelty in labrid fishes. Ecol. Lett. 14, 462-469. (doi:10.1111/j.1461-0248.2011. 01607.x)
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. (doi:10.1111/j.1420-9101.2011.02391.x)
Sorenson L, Santini F, Alfaro ME. 2014 The effect of habitat on modern shark diversification. J. Evol. Biol. 27, 1536-1548. (doi:10.1111/jeb.12405)
Price SA, Claverie T, Near TJ, Wainwright PC. 2015 Phylogenetic insights into the history and diversification of fishes on reefs. Coral Reefs 34, 997-1009. (doi:10.1007/s00338-015-1326-7)
Bellwood DR, Goatley CHR, Bellwood O. 2016 The evolution of fishes and corals on reefs: form, function and interdependence. Biol. Rev. (doi:10. 1111/brv.12259)
Santini F, Nguyen MTT, Sorenson L, Waltzek TB, Alfaro JWL, Eastman JM, Alfaro ME. 2013 Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae). J. Evol. Biol. 26, 1003-1018. (doi:10.1111/jeb.12112)
Betancur RR, Ortı´ G, Stein AM, Marceniuk AP, Alexander Pyron R. 2012 Apparent signal of competition limiting diversification after ecological transitions from marine to freshwater habitats. Ecol. Lett. 15, 822-830. (doi:10.1111/j.1461-0248.2012. 01802.x)
Kröger B, Yun-Bai Z. 2009 Pulsed cephalopod diversification during the Ordovician. Palaeogeogr. Palaeoclimatol. Palaeoecol. 273, 174-183. (doi:10.1016/j.palaeo.2008.12.015)
Slater GJ, Price SA, Santini F, Alfaro ME. 2010 Diversity versus disparity and the radiation of modern cetaceans. Proc. R. Soc. B 277, 3097-3104. (doi:10.1098/rspb.2010.0408)
Miya M et al. 2013 Evolutionary origin of the Scombridae (tunas and mackerels): members of a Paleogene adaptive radiation with 14 other pelagic fish families. PLoS ONE 8, e73535. (doi:10.1371/journal.pone.0073535)
Lobato FL, Barneche DR, Siqueira AC, Liedke AMR, Lindner A, Pie MR, Bellwood DR, Floeter SR. 2014 Diet and diversification in the evolution of coral reef fishes. PLoS ONE 9, e102094. (doi:10.1371/journal. pone.0102094)
Blake RW. 2004 Fish functional design and swimming performance. J. Fish Biol. 65, 1193-1222. (doi:10.1111/j.1095-8649.2004.00568.x)
Frédérich B, Olivier D, Litsios G, Alfaro ME, Parmentier E. 2014 Trait decoupling promotes evolutionary diversification of the trophic and acoustic system of damselfishes. Proc. R. Soc. B 281, 20141047. (doi:10.1098/rspb.2014.1047)
Marramà G, Garbelli C, Carnevale G. 2016 A morphospace for the Eocene fish assemblage of Bolca, Italy: a window into the diversification and ecological rise to dominance of modern tropical marine fishes. Boll. Soc. Pal. It. 55, 11-21.
Friedman M. 2010 Explosive morphological diversification of spiny-finned teleost fishes in the aftermath of the end-Cretaceous extinction. Proc. R. Soc. B 277, 1675-1683. (doi:10.1098/rspb. 2009.2177)
Eschmeyer WN, Fricke R, van der Laan R. 2016 Catalog of fishes (accessed July 2016). See http://research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp.
Santini F, Carnevale G. 2015 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. (doi:10.1016/j.ympev. 2014.10.018)
Froese R, Pauly D. 2015 FishBase (version 05/2015). See www.fishbase.org.
Collar DC, O’Meara BC, Wainwright PC, Near TJ. 2009 Piscivory limits diversification of feeding morphology in centrarchid fishes. Evolution 63, 1557-1573. (doi:10.1111/j.1558-5646.2009.00626.x)
Bannikov AF. 1990 Fossil carangids and apolectids of the USSR. Moscow, Russia: Nauka.
Blot J. 1969 Les poissons fossiles du Monte Bolca. Classés jusqu’ici dans les familles des Carangidae, Menidae, Ephippidae, Scatophagidae. Stud. Ric. Giaciam. Terz. Bolca 1, 1-525.
Friedman M, Johanson Z, Harrington RC, Near TJ, Graham MR. 2013 An early fossil remora (Echeneoidea) reveals the evolutionary assembly of the adhesion disc. Proc. R. Soc. B 280, 20131200. (doi:10.1098/rspb.2013.1200)
Zelditch ML, Swiderski DL, Sheets HD, Fink WL. 2004 Geometric morphometrics for biologists: a primer. San Diego, CA: Academic Press.
Rohlf FJ. 2004 TpsDig (version 1.40), a software program for landmark data acquisition. Department of Ecology and Evolution, State University of New York at Stony Brook. See http://life.bio.sunysb.edu/morph/.
Eloy C. 2013 On the best design for undulatory swimming. J. Fluid Mech. 717, 48-89. (doi:10. 1017/jfm.2012.561)
Harper DG, Blake RW. 1990 Fast-start performance of rainbow trout Salmo gairdneri and northern pike Esox Lucius. J. Exp. Biol. 150, 321-342.
Frédérich B, Sorenson L, Santini F, Slater GJ, Alfaro ME. 2013 Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae). Am. Nat. 181, 94-113. (doi:10.1086/668599)
Nelson JS. 2006 Fishes of the world. 4th edn. Hoboken, NJ: John Wiley & Sons.
Revell LJ. 2012 phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223. (doi:10. 1111/j.2041-210X.2011.00169.x)
R Development Core Team. 2011 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See http://R-project.org/.
Paradis E, Claude J, Strimmer K. 2004 APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290. (doi:10.1093/ bioinformatics/btg412)
Maddison WP, Midford PE, Otto SP. 2007 Estimating a binary character’s effect on speciation and extinction. Syst. Biol. 56, 701-710. (doi:10.1080/ 10635150701607033)
Beaulieu JM, O’Meara B. 2016 Detecting hidden diversification shifts in models of trait-dependent speciation and extinction. Syst. Biol. 65, 583-601. (doi:10.1093/sysbio/syw022)
Rabosky DL. 2010 Extinction rates should not be estimated from molecular phylogenies. Evolution 64, 1816-1824. (doi:10.1111/j.1558-5646.2009. 00926.x)
Burnham KP, Anderson DR. 2002 Model selection and multimodel inference: a practical information the oretic approach. New York, NY: Springer.
Beaulieu JM, Jhwueng D-C, Boettiger C, O’Meara BC. 2012 Modeling stabilizing selection: expanding the Ornstein-Uhlenbeck model of adaptive evolution. Evolution 66, 2369-2383. (doi:10.1111/j.1558-5646.2012.01619.x)
Adams DC, Otárola-Castillo E. 2013 Geomorph: an r package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393-399. (doi:10.1111/2041-210X.12035)
Hammer O, Harper DAT, Ryan PD. 2001 PAST: paleontological Statistics software package for education and data analysis. Palaeontol. Electron. 4, 1-9.
Claverie T, Wainwright PC. 2014 A morphospace for reef fishes: elongation is the dominant axis of body shape evolution. PLoS ONE 9, e112732. (doi:10.1371/journal.pone.0112732)
Friedman M. 2009 Ecomorphological selectivity among marine teleost fishes during the end-Cretaceous extinction. Proc. Natl Acad. Sci. USA 106, 5218-5223. (doi:10.1073/pnas.0808468106)
Ross ST. 1986 Resource partitioning in fish assemblages: a review of field studies. Copeia 1986, 352-368. (doi:10.2307/1444996)
Jennings S, Pinnegar JK, Polunin NVC, Boon TW. 2001 Weak cross-species relationships between body size and trophic level belie powerful sizebased trophic structuring in fish communities. J. Anim. Ecol. 70, 934-944. (doi:10.1046/j.0021-8790.2001.00552.x)
Domeneci P, Blake RW. 1997 The kinematics and performance of fish fast-start swimming. J. Exp. Biol. 200, 1165-1178.
Brönmark C, Miner JG. 1992 Predator-induced phenotypical change in body morphology in crucian carp. Science 258, 1348-1350. (doi:10.1126/ science.258.5086.1348)
Zhao S, Brady PC, Gao M, Ian Etheredge R, Kattawar GW, Cummings ME. 2015 Broadband and polarization reflectors in the lookdown, Selene vomer. J. R. Soc. Interface 12, 20141390. (doi:10. 1098/rsif.2014.1390)
Britz R, Johnson GD. 2012 Ontogeny and homology of the skeletal elements that form the sucking disc of remoras (Teleostei, Echeneoidei, Echeneidae). J. Morphol. 273, 1353-1366. (doi:10.1002/jmor. 20063)
Jacobs DK, Haney TA, Louie KD. 2004 Genes, diversity, and geologic process on the Pacific Coast. Annu. Rev. Earth Planet. Sci. 32, 601-652. (doi:10.1146/annurev.earth.32.092203.122436)
Grant KM, Dickens GR. 2002 Coupled productivity and carbon isotope records in the southwest Pacific Ocean during the late Miocene-early Pliocene biogenic bloom. Palaeogeogr. Palaeoclimatol. Palaeoecol. 187, 61-82. (doi:10.1016/S0031-0182(02)00508-4)
Santini F, Carnevale G, Sorenson L. 2013 First molecular scombrid timetree (Percomorpha: Scombridae) shows recent radiation of tunas following invasion of pelagic habitat. Ital. J. Zool. 80, 210-221. (doi:10.1080/ 11250003.2013.775366)
Santini F, Carnevale G, Sorenson L. 2014 First multilocus timetree of seabreams and porgies (Percomorpha: Sparidae). Ital. J. Zool. 81, 55-71. (doi:10.1080/11250003.2013.878960)
Frederich B, Marramà G, Carnevale G, Santini F. 2016 Data from: Non-reef environments impact the diversification of extant jacks, remoras and allies (Carangoidei, Percomorpha). Dryad Digital Repository. http://dx.doi.org/10.5061/ dryad.fs618.
