Pinniped phylogeny and a new hypothesis for their origin and dispersal

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Abstract

The relationships and the zoogeography of the three extant pinniped families, Otariidae (sea lions and fur seals), Odobenidae (one extant species, the walrus), and Phocidae (true seals), have been contentious. Here, we address these topics in a molecular study that includes all extant species of true seals and sea lions, four fur seals and the walrus. Contrary to prevailing morphological views the analyses conclusively showed monophyletic Pinnipedia with a basal split between Otarioidea (Otariidae + Odobenidae) and Phocidae. The northern fur seal was the sister to all remaining otariids and neither sea lions nor arctocephaline fur seals were recognized as monophyletic entities. The basal Phocidae split between Monachinae (monk seals and southern true seals) and Phocinae (northern true seals) was strongly supported. The phylogeny of the Phocinae suggests that the ancestors of Cystophora (hooded seal) and the Phocini (e.g. harp seal, ringed seal) adapted to Arctic conditions and ice-breeding before 12 MYA (million years ago) as supported by the white natal coat of these lineages. The origin of the endemic Caspian and Baikal seals was dated well before the onset of major Pleistocene glaciations. The current findings, together with recent advances in pinniped paleontology, allow the proposal of a new hypothesis for pinniped origin and early dispersal. The hypothesis posits that pinnipeds originated on the North American continent with early otarioid and otariid divergences taking place in the northeast Pacific and those of the phocids in coastal areas of southeast N America for later dispersal to colder environments in the N Atlantic and the Arctic Basin, and in Antarctic waters.

Introduction

The topic of pinniped biogeography was probably first addressed by Sclater (1897), who postulated origin of the group in southern oceans. This view, which had been seconded by von Boetticher (1934), was formally questioned by Davies (1958), who advocated pinniped origin in the Holarctic. Based on the working hypothesis that “The pinnipeds are, and always have been, generally tied to a cold-water environment”, Davies concluded that the pinnipeds had originated in the Arctic Basin, with the otarioids subsequently colonizing the N Pacific and the phocids the N Atlantic, before dispersing to other areas.

Davies (1958) had assumed monophyletic Pinnipedia in his study. That notion was gradually replaced, however, by a morphologically based view that favored pinniped diphyly with the otarioids sharing ancestry with the ursids and the phocids with the mustelids. This phylogenetic understanding also led to a revised pinniped biogeography, the essence of which was that early otarioid evolution had taken place in coastal areas of the N Pacific and that of the phocids in European waters.

Sarich (1969) challenged the notion of pinniped diphyly in an immunological study that unequivocally showed monophyletic Pinnipedia. This phylogeny has been recognized in essentially all later molecular analyses, irrespective of whether they have been based on nuclear data (de Jong and Goodman, 1982, Arnason and Widegren, 1986), complete mitochondrial (mt) genes (Arnason et al., 1995, Ledje and Arnason, 1996a, Ledje and Arnason, 1996b) or, more recently, on complete mt genomes (Arnason et al., 2002, Arnason and Janke, 2002, Davis et al., 2004, Delisle and Strobeck, 2005). The molecular recognition of pinniped monophyly gradually led to reconsideration of the morphological understanding favoring pinniped diphyly. However, these newer morphological studies (e.g. Wyss and Flynn, 1993, Berta and Wyss, 1994) did not support the traditionally accepted sister group relationship between Otariidae and Odobenidae (=Otarioidea), but rather advocated a sister group relationship between Phocidae and Odobenidae (=Phocomorpha) to the exclusion of Otariidae. This latter relationship was assumed as the basis of a recent proposal for pinniped biogeography (Deméré et al., 2002). More recently, Fyler et al. (2005) addressed some aspects of Monachinae biogeography. Some conclusions of this paper are inconsistent, however, with recent advances in phocid paleontology (e.g. Koretsky, 2001, Koretsky and Holec, 2002, Koretsky and Sanders, 2002).

In the current study, we reconsider pinniped evolution and biogeography using more extensive molecular data than previously available, and by taking into account paleontological evidence that has previously not been placed in a phylogenetic context of this kind. The analyses include 21 newly sequenced and 10 previously published pinniped mt genomes. The sampling includes all recent species of true seals and sea lions, four fur seals and the walrus. The analysis followed the now common practice of joining the sequences of 12 mitochondrial (mt) protein-coding genes of each species into one long sequence. This approach, introduced by Arnason and Johnsson (1992), expanded on by Janke et al. (1994) and extensively discussed by Paton and Baker (2006), rests on the demonstration that, while individual genes may yield different trees, longer genes and in particular the concatenated sequences of all genes result in trees that show consistency with well-supported non-molecular hypotheses.

The initial phase of the study aimed at establishing pinniped relationships. Thereafter the phylogenetic results, in conjunction with molecular datings and new paleontological and climatological findings, were used to elaborate the new hypothesis for pinniped biogeography.

Section snippets

Materials and methods

Table 1 lists the 39 species included in the study and the accession numbers of their complete mt genomes (when applicable). The accession numbers of the new genomes are shown in bold. The mt genome of the ringed seal, Phoca hispida, was sequenced using cloned restriction fragments from enriched mtDNA preparations. The preparation of enriched mtDNA followed the procedure briefly described in Arnason et al. (1991). Remaining genomes were PCR amplified, typically in 2–4 kb large fragments using

Pinniped phylogeny

The carnivore tree was rooted with two perissodactyls (the Indian rhino and the donkey), a group that has been shown to be closely related to the carnivores (Xu et al., 1996). The sampling includes two feliforms, the domestic cat and the cheetah, that were used to establish the split between the feliforms and the caniforms. Basal caniform relationships were recently examined using mitogenomic data (Delisle and Strobeck, 2005). These relationships are therefore not addressed here.

Fig. 1 shows

Acknowledgments

We express our gratitude to persons and institutes that provided us with samples (see Table 1) and to Jan Backman, Sylvia Brunner, John J. Flynn, Irina A. Koretsky, Kent Larsson, Ian A. McLaren, James G. Mead, Edward D. Mitchell, and Charles A. Repenning for valuable comments on the manuscript. The study was supported by The Swedish Research Council, The Nilsson-Ehle Foundation, The Erik Philip-Sörensen Foundation, and by EU Grant ERB-FMRX-CT98-0221.

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