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. 2009 Dec;58(6):573-85.
doi: 10.1093/sysbio/syp060. Epub 2009 Oct 5.

Radiation of extant cetaceans driven by restructuring of the oceans

Mette E Steeman  1 , Martin B Hebsgaard, R Ewan Fordyce, Simon Y W Ho, Daniel L Rabosky, Rasmus Nielsen, Carsten Rahbek, Henrik Glenner, Martin V Sørensen, Eske Willerslev
Affiliations

Radiation of extant cetaceans driven by restructuring of the oceans

Mette E Steeman et al. Syst Biol. 2009 Dec.

Abstract

The remarkable fossil record of whales and dolphins (Cetacea) has made them an exemplar of macroevolution. Although their overall adaptive transition from terrestrial to fully aquatic organisms is well known, this is not true for the radiation of modern whales. Here, we explore the diversification of extant cetaceans by constructing a robust molecular phylogeny that includes 87 of 89 extant species. The phylogeny and divergence times are derived from nuclear and mitochondrial markers, calibrated with fossils. We find that the toothed whales are monophyletic, suggesting that echolocation evolved only once early in that lineage some 36-34 Ma. The rorqual family (Balaenopteridae) is restored with the exclusion of the gray whale, suggesting that gulp feeding evolved 18-16 Ma. Delphinida, comprising all living dolphins and porpoises other than the Ganges/Indus dolphins, originated about 26 Ma; it contains the taxonomically rich delphinids, which began diversifying less than 11 Ma. We tested 2 hypothesized drivers of the extant cetacean radiation by assessing the tempo of lineage accumulation through time. We find no support for a rapid burst of speciation early in the history of extant whales, contrasting with expectations of an adaptive radiation model. However, we do find support for increased diversification rates during periods of pronounced physical restructuring of the oceans. The results imply that paleogeographic and paleoceanographic changes, such as closure of major seaways, have influenced the dynamics of radiation in extant cetaceans.

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Figures

F<sc>IGURE</sc> 1.
FIGURE 1.
Coastline maps indicating the timing of opening and closure of oceanic gateways. By 30 Ma, the Drake Passage and the Tasmanian Seaway had opened enough for the Antarctic Circumpolar Current to be established. At 12 Ma, the 3 major equatorial oceanic gateways, the Tethys Seaway, the IndoPacific Seaway, and the Central American Seaway, were still open. Between then and the present, these 3 equatorial gateways have been closed or restricted, inhibiting significant equatorial exchange between the Pacific, Atlantic, and Indian oceans. Maps are available from http://jan.ucc.nau.edu/ ∼ rcb7/ with permission.
F<sc>IGURE</sc> 2.
FIGURE 2.
Phylogeny of Cetacea, inferred using a Bayesian approach from a supermatrix of 15 mitochondrial and nuclear genes. A list of taxa and GenBank accession numbers is given in Appendix S1. Nodes are coded to indicate 3 levels of posterior probability as shown in the inset.
F<sc>IGURE</sc> 3.
FIGURE 3.
Molecular phylogeny of 87 recent cetacean species correlated with major global environmental changes. Chronogram obtained from a relaxed clock applied to the topology and branch lengths shown in Fig. 2. Estimated standard deviations are indicated on selected nodes with gray error bars. Clades undergoing increases in diversification rates (likelihood ratio-based shift statistics: P Llanocetus denticrenatus; 3, stem balaenid; 4, “Megaptera” miocena (phylogenetic position within crown Balaenopteridae uncertain); 5, Kentriodon ? sp.; 6, Brachydelphis mazeasi; and 7, Salumiphocaena stocktoni (see Appendix S2 for references). Blue areas represent periods of major oceanic restructuring (35–31 and 13-4 Ma) where the phylogeny was tested for changes in the diversification rate. Smoothed curves represent global ocean productivity (Zachos et al. 2001), sea-level fluctuations (Miller et al. 2005), and temperature (Zachos et al. 2001) across time, with times of opening and closure of major oceanic gateways (Kuhnt et al. 2004; Scher and Martin 2006; Harzhauser and Piller 2007; Jain and Collins 2007) given below.
F<sc>IGURE</sc> 4.
FIGURE 4.
Profile analysis of diversification rates in the Cetacea across the Cenozoic. a) Log likelihood of temporal change in diversification rates during the radiation of extant cetaceans. Results are based on a sliding window analysis with a fixed width of 6 Ma and suggest a shift in baseline diversification rates from 9–3 Ma. b) Speciation-through-time curve for extant Cetacea inferred using 6-Ma window. Results suggest elevated rates of speciation during the late Miocene–early Pliocene (9–4 Ma).
F<sc>IGURE</sc> 5.
FIGURE 5.
Log lineages-through-time plot for the cetacean radiation and generic diversity of genera through time. Palaeontological data are extracted from the Paleobiology Database (Uhen and Pyenson 2005).
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References

    1. Agnarsson I, May-Collado LJ. The phylogeny of Cetartiodactyla: the importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies. Mol. Phylogenet. Evol. 2008;48:964–985. - PubMed
    1. Ainley D, Ballard G, Ackley S, Blight LK, Eastman JT, Emslie SD, Lescroel A, Olmastron S, Townsend SE, Tynan CT, Wilson P, Woehler E. Paradigm lost, or is top-down forcing no longer significant in the Antarctic marine ecosystem? Antarct. Sci. 2007;19:283–290.
    1. Arnason U, Gullberg A. Relationship of baleen whales established by cytochrome b gene sequence comparison. Nature. 1994;367:726–728. - PubMed
    1. Arnason U, Gullberg A, Janke A. Mitogenomic analyses provide new insights into cetacean origin and evolution. Gene. 2004;333:27–34. - PubMed
    1. Barraclough TG, Vogler AP. Recent diversification rates in North American tiger beetles estimated from a dated mtDNA phylogenetic tree. Mol. Biol. Evol. 2002;19:1706–1716. - PubMed

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