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DNA Evidence for a Paleocene Origin of the Alcidae (Aves: Charadriiformes) in the Pacific and Multiple Dispersals Across Norther

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DNA Evidence for a Paleocene Origin of the Alcidae (Aves: Charadriiformes) in the Pacific and Multiple Dispersals Across Norther Available online at www.sciencedirect.com Molecular Phylogenetics and Evolution 46 (2008) 430–445 www.elsevier.com/locate/ympev DNA evidence for a Paleocene origin of the Alcidae (Aves: Charadriiformes) in the Pacific and multiple dispersals across northern oceans Sergio L. Pereira a,*, Allan J. Baker a,b a Department of Natural History, Royal Ontario Museum, 100 Queen’s Park Crescent, Toronto, Ont., Canada M5S 2C6 b Department of Ecology and Evolution, University of Toronto, Toronto, Ont., Canada M5S 1A1 Received 30 December 2006; revised 5 November 2007; accepted 27 November 2007 Available online 5 December 2007 Abstract The Alcidae is a group of marine, wing-propelled diving birds known as auks that are distributed along the coasts of the northern oceans. It has been suggested that auks originated in the Pacific coastal shores as early as the Miocene, and dispersed to the Atlantic either through the Arctic coasts of Eurasia and North America (northern dispersal route), or through upwelling zones in the coastal areas of California to Florida (southern dispersal route), before the closure of the Isthmus of Panama in the Pliocene. These hypotheses have not been tested formally because proposed phylogenies failed to recover fully bifurcating, well-supported phylogenetic relationships among and within genera. We therefore constructed a large data set of mitochondrial and nuclear DNA sequences for 21 of the 23 species of extant auks. We also included sequences from two other extant and one extinct species retrieved from GenBank. Our analyses recov- ered a well-supported phylogenetic hypothesis among and within genera. Aethia is the only genus for which we could not obtain strong support for species relationships, probably due to incomplete lineage sorting. By applying a Bayesian method of molecular dating that allows for rate variation across lineages and genes, we showed that auks became an independent lineage in the Early Paleocene and radi- ated gradually from the Early Eocene to the Quaternary. Reconstruction of ancestral areas strongly suggests that auks originated in the Pacific during the Paleocene. The southern dispersal route seems to have favored the subsequent colonization of the northern Atlantic Ocean during the Eocene and Oligocene. The northern route across the Arctic Ocean was probably only used more recently after the opening of the Norwegian Sea in the Middle Miocene and the opening of the Bering Strait in the Late Miocene. We postulate that the ancestors of auks lived in a warmer world than that currently occupied by auks, and became gradually adapted to feeding in cool marine currents with high biomass productivity. Hence, warmer tropical waters are now a barrier for the dispersal of auks into the Southern Hemisphere, as it is for penguins in the opposite direction. Ó 2007 Elsevier Inc. All rights reserved. Keywords: Alcidae; Divergence times; Molecular phylogenetics; Biogeography; Paleocene; Dispersal; Speciation; Pacific Ocean; Atlantic Ocean 1. Introduction auks. They come to land briefly to reproduce, usually in rocks and cliffs in offshore islands and narrow coastal strips The Alcidae is a group of 23 extant and one recently that are hardly accessed by land predators (Gaston and extinct species of marine, wing-propelled diving birds that Jones, 1998). spend most of their lives foraging in the northern seas of Based on the age and diversity of forms observed in the the Northern Hemisphere and are collectively known as marine fossil record it has been hypothesized that auks originated in the Pacific region (Gaston and Jones, 1998; Olson, 1985). Hydrotherikornis from the Late Eocene of * Corresponding author. Fax: +1 416 586 5553. Oregon is the oldest fossil that has been attributed to the E-mail address: [email protected] (S.L. Pereira). Alcidae, but the first undisputed fossils of the group are 1055-7903/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2007.11.020 S.L. Pereira, A.J. Baker / Molecular Phylogenetics and Evolution 46 (2008) 430–445 431 the extinct genera Alcodes (Howard, 1968)andMiocepphus 1996a; Moum et al., 1994), incomplete taxon sampling (Olson, 1985) from marine deposits of the Middle Miocene (Moum et al., 2002; Watada et al., 1987), and contentious of the Pacific and Atlantic Oceans, respectively. Later on, treatment of clades shared among multiple phylogenetic the extinct genus Praemancalla and forms possibly related source trees as characters (supertree approaches) (Thomas to modern Cepphus, Cerorhinca, Aethia and Uria appear in et al., 2004). marine deposits of the Late Miocene of the Pacific. The In the present study, we aimed to fully resolve the phy- extinct genus Australca and modern Alca, Alle, Fratercula logenetic relationships of all the genera and species of the and Pinguinus appear in the marine fossil record of Atlantic Alcidae with a much larger data set of DNA sequences deposits of the Late Miocene and Pliocene. If auks origi- than were used in previous studies. We used the statistically nated as far back as at least the Miocene, it is very likely best-supported tree topology to estimate divergence times that their radiation began in the Pacific Ocean and they and areas where ancestors of the Alcidae may have origi- became adapted to marine environments early in their evo- nated. This is the first study to test the hypothesis of a Paci- lutionary history. During the Miocene, the Pacific would fic origin and alternative hypotheses for their dispersal have provided a greater expanse for the evolution of mar- routes within a strong phylogenetic framework using mod- ine birds compared to the Northern Atlantic Ocean, which ern methods of tree inference, molecular dating and ances- was still in the process of opening up during the end of the tral area reconstruction. Our estimates are interpreted Eocene and throughout the Oligocene (Olson, 1985). based on the geological history of the Northern Hemi- From the Pacific, auks are thought to have colonized the sphere throughout the Cenozoic. Atlantic and Arctic Oceans, but competing hypotheses have been proposed to explain possible colonization routes. 2. Materials and methods One hypothesis posits that they crossed the Bering Strait into the Arctic Ocean, and reached the Atlantic region 2.1. Taxon sampling, DNA amplification, sequencing and via the Arctic coasts of Eurasia and North America sequence alignments (Be´dard, 1985). New geological evidence for reduced salin- ity and increased freshwater input in the Arctic Ocean dur- Twenty (87%) out of the 23 recognized extant species ing the Eocene (Brinkhuis et al., 2006) would make this within the Alcidae, and three other Charadriiformes out- dispersal route more unlikely if the ancestors of auks were groups were sampled for this study (Table 1). DNA was already adapted to marine environments. On the other isolated following standard protocols (Sambrook et al., hand, an alternative colonization route has been suggested 1989). Mitochondrial and nuclear DNA amplifications via the Pacific southern coasts of North America to the were carried out for the small and large ribosomal subunit Atlantic before North and South America finally became (12S and 16S rDNA, respectively), NADH dehydrogenase connected to each other through the Isthmus of Panama subunit 2 (ND2), cytochrome b (cyt b) (primers designed by (Konyukhov, 2002). This hypothesis also postulates that O. Haddrath and described in Pereira and Baker, 2004b) the exchange between the Atlantic and the Pacific Oceans and cytochrome c oxidase subunit I (COI) (COIaR—aac occurred more recently, through periodic openings of the yaa cca caa aga cat ygg and COIbR—gan agg aca tag Bering Strait from the Late Miocene to the Pleistocene tgg aag tgg gc; O. Haddrath, personal communication), (Konyukhov, 2002). and the nuclear recombination activating protein (RAG- The lack of a well-supported phylogenetic hypothesis at 1) gene (primer combinations R13 and R18, R17 and the genus and species level has precluded further testing of R22, and R21 and R2b in Groth and Barrowclough, the proposed hypotheses for their center of origin and dis- 1999), following published protocols (Groth and Barrowc- persal routes. Published phylogenies (Fig. 1) agree that the lough, 1999; Pereira and Baker, 2005). After amplification, auks can be subdivided in two major sister clades (Friesen PCR products were separated in and recovered from 1% et al., 1996a; Moum et al., 2002, 1994; Strauch, 1985; Tho- agarose gels, purified by centrifuging each recovered frag- mas et al., 2004; Watada et al., 1987). One of the major ment through a filter tip, cycle-sequenced and run on a clades includes puffins (Fratercula) and auklets (Cerorhin- Li-Cor 4200 bidirectional automated DNA sequencer ca, Aethia and Ptychoramphus) that feed mainly on zoo- according to the manufacturer’s suggested protocol. Both plankton, and the other contains murres (Uria), murrelets L- and H-strands sequences were checked for ambiguities (Brachyramphus and Synthliboramphus), guillemots (Cep- and final consensus sequences were created for each frag- phus), Dovekie (Alle alle), Razorbill (Alca torda) and the ment sequenced in Sequencher 4.1.2 (GeneCOdes Corp., recently extinct Great Auk (Pinguinus impennis) that feed Inc., Ann Arbor, Michigan). Consensus sequences plus primarily on fishes. However, these same phylogenies have sequences for alcids retrieved from GenBank (Table 1), failed to provide strong support for the generic and some including Cepphus grylle, Synthliboramphus hypoleucus of the specific relationships within the family mainly due and the extinct Great Auk Pinguinus impennis for which to use of characters under natural selection and prone to we did not have DNA samples, were aligned visually in convergent evolution at the genotypic and phenotypic lev- MacClade 4.0 (Maddison and Maddison, 2000). A final els (Friesen et al., 1996b; Strauch, 1985; Watada et al., matrix of 7403 base pairs (bp), including gaps, was used 1987), insufficient character sampling (Friesen et al., for phylogenetic analyses. New sequences obtained in this 432 S.L.
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