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Phylogenetic Relationships of the Extinct Sthelena Petrel, Pterodroma

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Phylogenetic Relationships of the Extinct Sthelena Petrel, Pterodroma bs_bs_banner Zoological Journal of the Linnean Society, 2013. With 2 figures Phylogenetic relationships of the extinct St Helena petrel, Pterodroma rupinarum Olson, 1975 (Procellariiformes: Procellariidae), based on ancient DNA ANDREANNA J. WELCH1,*, STORRS L. OLSON2 and ROBERT C. FLEISCHER3 1Department of Biological Sciences, University at Buffalo, Buffalo, NY 14260, USA 2Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA 3Smithsonian Conservation Biology Institute, Center for Conservation and Evolutionary Genetics, National Zoological Park, Washington, DC 20013, USA Received 9 May 2013; revised 29 July 2013; accepted for publication 2 August 2013 Palaeontological studies show that three endemic procellariid seabird species became extinct on the remote island of St Helena in the South Atlantic Ocean. At least one of these, Pterodroma rupinarum Olson, 1975, is likely to have survived until human colonization of the island, although it is known only from subfossil bones. Several species of Pterodroma are distributed across the Atlantic, but the skull and bill of Pt. rupinarum were judged to be more similar to the Indo-Pacific Pterodroma rostrata group, which was recently split into the separate genus Pseudobulweria. We used ancient DNA techniques to sequence the mitochondrial cytochrome b gene of the extinct Pt. rupinarum, and conducted phylogenetic analyses to investigate the placement of this enigmatic taxon. In trees constructed using maximum likelihood and Bayesian inference, Pt. rupinarum did not group with Pseudobulweria, but instead fell within a strongly supported clade of Atlantic Pterodroma, including the endangered Black-capped [Pterodroma hasitata (Kuhl, 1820)] and Bermuda [Pterodroma cahow (Nichols & Mowbray, 1916)] petrels, as well as the Macaronesian petrels [Pterodroma madeira Mathews, 1934, Pterodroma feae (Salvadori, 1899) and Pterodroma deserta Mathews, 1934]. Pterodroma rupinarum shared a particularly close relationship with Pt. feae of the Cape Verde Islands, which is also the geographically closest species within the clade. Considering the osteological distinctiveness of Pt. rupinarum it was probably a separate species, or at least a highly diverged population that was isolated for a substantial period of time prior to its extinction. © 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013 doi: 10.1111/zoj.12078 ADDITIONAL KEYWORDS: cytochrome b – extinction – petrel – phylogeny – Pseudobulweria – Pterodroma – St Helena. INTRODUCTION thousands of kilometers on a single foraging trip during the breeding season (Brooke, 2004). Their Seabirds are highly vagile, and may forage widely ability to disperse widely over expansive pelagic eco- over the open oceans, travelling hundreds to systems makes them a useful indicator of marine conditions (Piatt, Sydeman & Wiese, 2007; Wiley et al., 2013), and as top marine predators they play *Corresponding author. Current address: School of ecologically important roles (Sánchez-Piñero & Polis, Biological and Biomedical Sciences, Durham University, UK; Institute of Marine Sciences, University of California, Santa 2000; Croll et al., 2005). Unfortunately, seabirds are Cruz, CA, USA. E-mail: [email protected] one of the most endangered groups of birds in the © 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013 1 2 A. J. WELCH ET AL. world (Croxall et al., 2012). The family Procellariidae Fossils from Saint Helena, a remote island in the contains approximately 80 species of petrels and South Atlantic Ocean (Fig. 1), showed that three shearwaters, although the taxonomy of this group is apparently endemic species of Procellariidae became challenging and often disputed (Brooke, 2004; extinct there, and populations of three other pro- Penhallurick & Wink, 2004; Rheindt & Austin, 2005). cellariids, along with several additional species of The Procellariidae ranks as the third most endan- seabirds, were extirpated (Olson, 1975). Of the three gered seabird family (Croxall et al., 2012), and many extinct species, only one, Puffinus pacificoides Olson, of these species face substantial threats both at the 1975, is likely to have disappeared prior to human breeding grounds as well as at sea (Weimerskirch, arrival, probably during the Pleistocene. Another Brothers & Jouventin, 1997; Lewison & Crowder, species, Bulweria bifax Olson, 1975, was much 2003; Wanless et al., 2007; Fontaine, Gimenez & more abundant in the Pleistocene than in recent Bried, 2011; Barbraud et al., 2012). Despite this, deposits, and may have been decreasing in number investigation of the fossil record indicates that in the towards modern times. The third species, Pterodroma recent past seabird extinction has been relatively rupinarum Olson, 1975, was fairly common in the rare, especially when compared with the extinction most recent deposits, and may have become extinct rate of terrestrial species on oceanic islands after the discovery of the island in 1502 by Portu- (Steadman, 1995; Steadman, 2006). guese sailors (Olson, 1975). Little is known about the P. cahow P. deserta P. madeira P. hasitata P. caribbaea† P. feae P. rupinarum † P. arminjoniana P. mollis P. incerta Figure 1. Approximate recent breeding locations of Pterodroma petrels in the Atlantic Ocean. © 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013 ST HELENA PETREL, PTERODROMA RUPINARUM 3 avifauna of St Helena at the time of human coloniza- this species in a phylogeny including nearly all tion, as there appear to be no written accounts from Pterodroma and Pseudobulweria petrels. that period; however, after permanent settlement in 1513 there are numerous accounts of large numbers of feral invasive species, including goats, pigs, rats, MATERIAL AND METHODS mice, and cats (Gosse, 1938), which would presum- ably have caused severe environmental perturbation SAMPLES AND MOLECULAR TECHNIQUES and led to greatly increased predation on burrow- Of the thousands of available bones of Pt. rupinarum nesting seabirds. collected by Olson in 1971, ten were selected from Initial work by Bourne (1956) on the taxonomic three sites on St Helena: eight from Prosperous Bay identification of a limited number of Pterodroma (USNM 176607, 176608, 176610, 176613, 176615, bones from St Helena ruled out affinity with 176623, 176627, 176641), one from Sandy Bay Pterodroma arminjoniana (Giglioli & Salvadori, (USNM 176679), and one from Sugarloaf Hill, site 2 1869), the only other tropical South Atlantic petrel (USNM 176702). Bones that were clearly identifiable (Fig. 1). Instead, he suggested that the fossils might as Pt. rupinarum were selected based on size, thick- belong to Macaronesian species of Pterodroma ness of bone walls, and un-weathered appearance. breeding on Madeira and the Cape Verde Islands A mixture of complete and partial elements was in the North Atlantic. Recent genetic work on the selected to minimize the effects of destructive sam- Macaronesian petrels suggests the existence of three pling. The age of the samples is not certainly known, recently diverged species: Pterodroma feae (Salvadori, but all of the deposits are thought to be late Holocene. 1899) in the Cape Verde archipelago; Pterodroma A small piece of bone (approximately 4 mm×6mm) deserta Mathews, 1934 on Bugio Island (first sug- was cut from each specimen using a rotary saw with gested as a distinct species by Bourne in 1955); and disposable blades. Each sample was ground into Pterodroma madeira Mathews, 1934 on the island of powder using a mortar and pestle and DNA was Madeira in the Madeira Archipelago (Fig. 1), although extracted using a phenol/chloroform procedure with the species status of Pt. deserta is still somewhat centrifugal dialysis (Fleischer et al., 2000). All labora- controversial (Zino, Brown & Biscoito, 2008; Jesus tory work was conducted in a physically isolated et al., 2009; Gangloff et al., 2013). Bourne (1965) facility dedicated for ancient DNA work, and strict later suggested that the fossil Pterodroma from protocols were followed to prevent contamination St Helena might belong with the Pterodroma rostrata from modern sources. Ancient DNA was extracted in group instead. Examination of greatly expanded batches of six samples, each of which included an material collected by Olson (1975) resulted in the extraction control. naming of the fossils as a new species, Pt. rupinarum, Most phylogenetic work on procellariiform seabirds some characters of which, particularly the skull has focused on the mitochondrial cytochrome b gene and the angle of the bill, were considered to be (Bretagnolle et al., 1998; Nunn & Stanley, 1998; more similar to the Pterodroma rostrata group Austin, Bretagnolle & Pasquet, 2004; Gangloff than to other Pterodroma petrels. Genetic work et al., 2012), so we targeted that gene for our study. (Bretagnolle, Attié & Pasquet, 1998) has since shown Polymerase chain reaction (PCR) was carried out that the Pterodroma rostrata group actually repre- as described in Welch et al. (2012). Briefly, PCR sents a distinct genus, Pseudobulweria, first proposed was conducted in 25-μL reaction volumes with 1 by Mathews in 1936 [type species Thalassidroma unit Amplitaq Gold DNA polymerase (Applied (Bulweria) macgillivrayi G.R. Gray, 1859]. The Biosystems), 2–3 μL of DNA extract, and with a total Indo-Pacific genus Pseudobulweria contains four of 45 cycles. We used a series of short (120–200 bp), extant species: Pseudobulweria
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