Abstract
Modern whales are frequently described as an adaptive radiation spurred by either the evolution of various key innovations (such as baleen or echolocation) or ecological opportunity following the demise of archaic whales. Recent analyses of diversification rate shifts on molecular phylogenies raise doubts about this interpretation since they find no evidence of increased speciation rates during the early evolution of modern taxa. However, one of the central predictions of ecological adaptive radiation is rapid phenotypic diversification, and the tempo of phenotypic evolution has yet to be quantified in cetaceans. Using a time-calibrated molecular phylogeny of extant cetaceans and a morphological dataset on size, we find evidence that cetacean lineages partitioned size niches early in the evolutionary history of neocetes and that changes in cetacean size are consistent with shifts in dietary strategy. We conclude that the signature of adaptive radiations may be retained within morphological traits even after equilibrium diversity has been reached and high extinction or fluctuations in net diversification have erased any signature of an early burst of diversification in the structure of the phylogeny.
References
-
Alfaro M. E., Santini F., Brock C., Alamillo H., Dornburg A., Rabosky D. L., Carnevale G.& Harmon L. J. . 2009 Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Natl Acad. Sci. USA 106, 13 410–13 414. (doi:10.1073/pnas.0811087106). Crossref, Web of Science, Google Scholar -
Berta A., Sumich J. L.& Kovacs K. M. . 2006 Marine mammals: evolutionary biology, 2nd edn. San Diego, CA: Associated Press. Google Scholar -
Bigg M. A., Olesiuk P. F., Ellis G. M., Ford J. K. B.& Balcomb K. C. . 1990 Social organization and genealogy of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State. Rep. Int. Whal. Comm. 12, 383–405. Google Scholar -
Burnham K. P.& Anderson D. R. . 2002 Model selection and multimodel inference: a practical information-theoretic approach. New York, NY: Springer. Google Scholar -
Clementz M., Goswami A., Gingerich P.& Koch P. . 2006 Isotopic records from early whales and sea cows: contrasting patterns of ecological transition. J. Vertebr. Paleontol. 26, 355–370. (doi:10.1671/0272-4634(2006)26[355:IRFEWA]2.0.CO;2). Crossref, Web of Science, Google Scholar -
Drummond A. J.& Rambaut A. . 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 1–8. Crossref, PubMed, Web of Science, Google Scholar -
Felsenstein J. . 1985 Phylogenies and the comparative method. Am. Nat. 126, 1–25. Crossref, Web of Science, Google Scholar -
Fordyce R. E. . 1992 Cetacean evolution and Eocene/Oligocene environments. Eocene–Oligocene climatic and biotic evolution (eds, Prothero D. R.& Berggren W. ). Princeton, NJ: Princeton University Press. Google Scholar -
Fordyce R. E. . 2003 Cetacean evolution and Eocene–Oligocene oceans revisited. From greenhouse to icehouse: the marine Eocene–Oligocene transition (eds, Prothero D. R., Ivany L. C.& Nesbitt E. R. ), pp. 154–170. New York, NY: Columbia University Press. Google Scholar -
Fordyce R. E.& Barnes L. G. . 1994 The evolutionary history of whales and dolphins. Annu. Rev. Earth Planet Sci. 22, 419–455. (doi:10.1146/annurev.ea.22.050194.002223). Crossref, Web of Science, Google Scholar -
Fordyce R. E.& de Muizon C. . 2001 Evolutionary history of whales: a review. Secondary adaptation of tetrapods to life in water. Proc. Int. Meeting, Poitiers 1996 (eds, Mazin J.-M.& de Buffrenil V. ), pp. 169–234. Munich, Germany: Verlag Dr Friedriech Pfeil. Google Scholar -
Freckleton R. P.& Harvey P. H. . 2006 Detecting non-Brownian trait evolution in adaptive radiations. PLoS Biol. 4, e373. (doi:10.1371/journal.pbio.0040373). Crossref, PubMed, Web of Science, Google Scholar -
Gavrilets S.& Losos J. B. . 2009 Adaptive radiation: contrasting theory with data. Science 323, 732–737. (doi:10.1126/science.1157966). Crossref, PubMed, Web of Science, Google Scholar -
Givnish T.& Sytsma K. . 1997 Molecular evolution and adaptive radiation. New York, NY: Cambridge University Press. Google Scholar -
Hansen T. F. . 1997 Stabilizing selection and the comparative analysis of adaptation. Evolution 51, 1341–1351. (doi:10.2307/2411186). Crossref, PubMed, Web of Science, Google Scholar -
Harmon L., Schulte J., Larson A.& Losos J. . 2003 Tempo and mode of evolutionary radiation in iguanian lizards. Science 301, 961–964. (doi:10.1126/science.1084786). Crossref, PubMed, Web of Science, Google Scholar -
Harmon L., Weir J., Brock C., Glor R.& Challenger W. . 2008 Geiger: investigating evolutionary radiations. Bioinformatics 24, 129–131. (doi:10.1093/bioinformatics/btm538). Crossref, PubMed, Web of Science, Google Scholar -
Heide-Jørgensen M. P., Bloch D., Stefansson E., Mikkelsen B., Ofstad L. H.& Dietz R. . 2002 Diving behaviour of long-finned pilot whales Globicephala melas around the Faroe Islands. Wildl. Biol. 8, 307–313. Crossref, Web of Science, Google Scholar -
Jarman P. J. . 1974 The social organisation of antelope in relation to their ecology. Behaviour 48, 215–267. (doi:10.1163/156853974X00345). Crossref, Web of Science, Google Scholar -
LaBarbara M. . 1989 Analyzing body size as a factor in ecology and evolution. Annu. Rev. Ecol. Syst. 20, 97–117. (doi:10.1146/annurev.es.20.110189.000525). Crossref, Google Scholar -
Losos J. B. . 2009 Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. Berkeley, CA: University of California Press. Crossref, Google Scholar -
Maddison W. P.& Maddison D. R. . 2009 Mesquite: a modular system for evolutionary analysis, v. 2.72. See http://mesquiteproject.org. Google Scholar -
Marino L., Sol D., Toren K.& Lefebvre L. . 2006 Does diving limit brain size in cetaceans? Mar. Mammal. Sci. 22, 413–425. (doi:10.1111/j.1748-7692.2006.00042.x). Crossref, Web of Science, Google Scholar -
McGowen M. R., Spaulding M.& Gatesy J. . 2009 Divergence date estimation and a comprehensive molecular tree of extant cetaceans. Mol. Phylogenet. Evol. 53, 891–906. (doi:10.1016/j.ympev.2009.08.018). Crossref, PubMed, Web of Science, Google Scholar -
McPeek M. A. . 1995 Testing hypotheses about evolutionary change on single branches of a phylogeny using evolutionary contrasts. Am. Nat. 45, 686–703. Crossref, Web of Science, Google Scholar -
Mead J. G.& Brownell R. L. . 2005 Order Cetacea. Mammal species of the world: a taxonomic and geographic reference (eds, Wilson D. E.& Reeder D. M. ), 3rd edn, pp. 723–743. Baltimore, MD: Johns Hopkins University Press. Google Scholar -
Noren S.& Williams T. . 2000 Body size and skeletal muscle myoglobin of cetaceans: adaptations for maximizing dive duration. Comp. Biochem. Phys. A 126, 181–191. Crossref, PubMed, Web of Science, Google Scholar -
Olson M. E.& Arroyo-Santos A. . 2009 Thinking in continua: beyond the ‘adaptive radiation’ metaphor. BioEssays 31, 1337–1346. (doi:10.1002/bies.200900102). Crossref, PubMed, Web of Science, Google Scholar -
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). Crossref, PubMed, Web of Science, Google Scholar -
Pybus O.& Harvey P. . 2000 Testing macro-evolutionary models using incomplete molecular phylogenies. Proc. R. Soc. Lond. B 267, 2267–2272. (doi:10.1098/rspb.2000.1278). Link, Web of Science, Google Scholar -
Quental T. B.& Marshall C. R. . 2009 Extinction during evolutionary radiations: reconciling the fossil record with molecular phylogenies. Evolution 63, 3158–3167. (doi:10.1111/j.1558-5646.2009.00794.x). Crossref, PubMed, Web of Science, Google Scholar -
Rabosky D. . 2006 Laser: a maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Evol. Bioinform. 2, 247–250. Crossref, Web of Science, Google Scholar -
Rabosky D.& Lovette I. . 2008 a Density-dependent diversification in North American wood warblers. Proc. R. Soc. B 275, 2363–2371. (doi:10.1098/rspb.2008.0630). Link, Web of Science, Google Scholar -
Rabosky D.& Lovette I. . 2008 b Explosive evolutionary radiations: decreasing speciation or increasing extinction through time? Evolution 62, 1866–1875. (doi:10.1111/j.1558-5646.2008.00409.x). Crossref, PubMed, Web of Science, Google Scholar -
Rabosky D. L., Donnellan S. C., Talaba A. L.& Lovette I. J. . 2007 Exceptional among-lineage variation in diversification rates during the radiation of Australia's most diverse vertebrate clade. Proc. R. Soc. B 274, 2915–2923. (doi:10.1098/rspb.2007.0924). Link, Web of Science, Google Scholar -
Schluter D. . 2000 The ecology of adaptive radiation. Oxford, UK: Oxford University Press. Google Scholar -
Simpson G. G. . 1944 The tempo and mode in evolution. New York, NY: Columbia University Press. Google Scholar -
Steeman M. E., 2009 Radiation of extant cetaceans driven by restructuring of the oceans. Syst. Biol. 58, 573–585. (doi:10.1093/sysbio/syp060). Crossref, PubMed, Web of Science, Google Scholar -
Thomas G. H., Freckleton R. P.& Székely T. . 2006 Comparative analyses of the influence of developmental mode on phenotypic diversification rates in shorebirds. Proc. R. Soc. B 273, 1619–1624. (doi:10.1098/rspb.2006.3488). Link, Web of Science, Google Scholar -
Thomas G. H., Meiri S.& Phillimore A. B. . 2009 Body size diversification in Anolis: novel environment and island effects. Evolution 63, 2017–2030. (doi:10.1111/j.1558-5646.2009.00694.x). Crossref, PubMed, Web of Science, Google Scholar -
Uhen M. D. . 2010 Cetacea online systematics archive 11. The paleobiology database, http://paleodb.org/cgi-bin/bridge.pl?user=Guest&action=displayPage&page=OSA_Cetacea. Google Scholar -
Uhen M. D.& Pyenson N. D. . 2007 Diversity estimates, biases, and historiographic effects: resolving cetacean diversity in the Tertiary. Palaeontol. Electron. 10, 1–22. Web of Science, Google Scholar -
Van Valkenburgh B., Wang X.& Damuth J. . 2004 Cope's rule, hypercarnivory, and extinction in North American canids. Science 306, 101–104. (doi:10.1126/science.1102417). Crossref, PubMed, Web of Science, Google Scholar -
Watkins W. A., Moore K. E.& Tyack P. . 1985 Investigations of sperm whale acoustic behaviors in the southeast Caribbean. Cetology 49, 1–15. Google Scholar -
Watkins W. A., Daher M. A., Fristrup K. M., Howald T. J.& Notarbartolo di Sciara G. . 1993 Sperm whales tagged with transponders and tracked underwater by sonar. Mar. Mam. Sci. 9, 55–67. (doi:10.1111/j.1748-7692.1993.tb00426.x). Crossref, Web of Science, Google Scholar -
Whitehead H.& Mann J. . 2000 Female reproductive strategies in cetaceans. Cetacean societies: field studies of dolphins and whales (eds, Mann J., Connor R. C., Tyack P. L.& Whitehead P. L. H. ), pp. 219–246. Chicago, IL: University of Chicago Press. Google Scholar