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A Molecular Phylogeny of Anseriformes Based on Mitochondrial DNA Analysis

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A Molecular Phylogeny of Anseriformes Based on Mitochondrial DNA Analysis MOLECULAR PHYLOGENETICS AND EVOLUTION Molecular Phylogenetics and Evolution 23 (2002) 339–356 www.academicpress.com A molecular phylogeny of anseriformes based on mitochondrial DNA analysis Carole Donne-Goussee,a Vincent Laudet,b and Catherine Haanni€ a,* a CNRS UMR 5534, Centre de Genetique Moleculaire et Cellulaire, Universite Claude Bernard Lyon 1, 16 rue Raphael Dubois, Ba^t. Mendel, 69622 Villeurbanne Cedex, France b CNRS UMR 5665, Laboratoire de Biologie Moleculaire et Cellulaire, Ecole Normale Superieure de Lyon, 45 Allee d’Italie, 69364 Lyon Cedex 07, France Received 5 June 2001; received in revised form 4 December 2001 Abstract To study the phylogenetic relationships among Anseriformes, sequences for the complete mitochondrial control region (CR) were determined from 45 waterfowl representing 24 genera, i.e., half of the existing genera. To confirm the results based on CR analysis we also analyzed representative species based on two mitochondrial protein-coding genes, cytochrome b (cytb) and NADH dehydrogenase subunit 2 (ND2). These data allowed us to construct a robust phylogeny of the Anseriformes and to compare it with existing phylogenies based on morphological or molecular data. Chauna and Dendrocygna were identified as early offshoots of the Anseriformes. All the remaining taxa fell into two clades that correspond to the two subfamilies Anatinae and Anserinae. Within Anserinae Branta and Anser cluster together, whereas Coscoroba, Cygnus, and Cereopsis form a relatively weak clade with Cygnus diverging first. Five clades are clearly recognizable among Anatinae: (i) the Anatini with Anas and Lophonetta; (ii) the Aythyini with Aythya and Netta; (iii) the Cairinini with Cairina and Aix; (iv) the Mergini with Mergus, Bucephala, Melanitta, Callonetta, So- materia, and Clangula, and (v) the Tadornini with Tadorna, Chloephaga, and Alopochen. The Tadornini diverged early on from the Anatinae; then the Mergini and a large group that comprises the Anatini, Aythyini, Cairinini, and two isolated genera, Chenonetta and Marmaronetta, diverged. The phylogeny obtained with the control region appears more robust than the one obtained with mitochondrial protein-coding genes such as ND2 and cytb. This suggests that the CR is a powerful tool for bird phylogeny, not only at a small scale (i.e., relationships between species) but also at the family level. Whereas morphological analysis effectively resolved the split between Anatinae and Anserinae and the existence of some of the clades, the precise composition of the clades are different when morphological and molecular data are compared. Ó 2002 Elsevier Science (USA). All rights reserved. Keywords: Anseriformes; mtDNA; Control region; Waterfowl 1. Introduction North America (Olson and Feduccia, 1980). According to these paleontological data, the main radiation of Among avian orders, the Anseriformes (screamers modern ducks has taken place during Miocene, 5–23 and waterfowls) are a morphologically and biologically million years ago (Olson, 1985). diverse group containing ca. 150 species distributed The Anseriformes are traditionally divided into two worldwide. This order contains the screamers of South families, Anhimidae (2 genera and 3 species) and America, the magpie goose of Australia and Asia, and Anatidae (approximately 41 genera and 147 species). the ducks, geese, and swans known worldwide. Fossil The taxonomic division is rather complex and has been records indicate that the first Anseriformes (genus much disputed and revised. Most available data con- Presbyornis) was present during Upper Paleocene (61– cerning Anseriformes phylogeny came from morpho- 62 million years ago), whereas the first Anatidae was logical, anatomical, and behavioral analyses (Delacour found in the Upper Eocene (40–50 million years ago) in and Mayr, 1945; Del Hoyo et al., 1992; Livezey, 1986, 1997b). Molecular data such as DNA–DNA hybridiza- * Corresponding author. Fax: +33-4-72-44-05-55. tion studies were also used to decipher the relationships E-mail address: [email protected] (C. Ha¨nni). between these birds (Sibley and Ahlquist, 1990). More 1055-7903/02/$ - see front matter Ó 2002 Elsevier Science (USA). All rights reserved. PII: S1055-7903(02)00019-2 340 C. Donne-Gousse et al. / Molecular Phylogenetics and Evolution 23 (2002) 339–356 recently, phylogenies based on DNA sequence analysis nae (Fig. 1B). A radically different view has been pro- of mitochondrial genes were proposed for some taxa of posed by Sibley and Ahlquist (1990), who cluster together the Anseriformes such as the Australasian waterfowl Chauna and Anseranas to form the suborder Anhimides. (Sraml et al., 1996), the genus Anas (Johnson and As Livezey (1997b), these authors consider Dendrocygna Sorenson, 1998, 1999), some extinct species such as an independent lineage. Because of these discrepancies moa-nalos (Sorenson et al., 1999a), or the endangered the composition of the family Anatidae is still a matter of Laysan ducks (Cooper et al., 1996). The phylogenies discussion, as for example the inclusion of Anseranas. obtained by these different approaches differ mostly on The Anatidae have been traditionally divided into two (i) the relative positions of Anhimidae (with Ansera- subfamilies, Anatinae and Anserinae, the latter including natidae) and Anatidae, (ii) the grouping of Anatidae in geese, swans, and Dendrocygna (Delacour and Mayr, two main subfamilies, Anatinae and Anserinae, and (iii) 1945; Del Hoyo et al., 1992; Fig. 1A and Appendix A). the phylogeny inside each of these subfamilies, in par- This view as been challenged by Livezey (1997b), who ticular the composition and relationships of so-called recognized four main clades (Fig. 1B): (i) the Anatinae; ‘‘tribes’’ clustering several genera within Anatidae. (ii) a clade called Tadornini including the genera Tad- The traditional classification of the Anseriformes of orna, Chloephaga, and Alopochen; (iii) the Anserinae; and Delacour and Mayr (1945), based on morphological and (iv) Dendrocygna. In addition other minor clades (Tha- behavioral characters, later modified by Johnsgard lassorninae, Stictonettinae, and Plectropterinae) were (1978), has been followed by many others (Del Hoyo et al., also noticed inside Anatidae. The relationships between 1992). According to these authors, the genus Chauna, all these clades remain poorly resolved. According to this representative of the Anhimidae, diverged first, and was author, the Tadornini, which were previously included then followed by Anseranas and the crown group con- inside the Anatinae by Del Hoyo et al. (1992), represent taining ducks, geese, and swans (Fig. 1A and Appendix an independent lineage. The definition of Anserinae by A). According to these authors the whistling-ducks Del Hoyo et al. (1992) and Livezey (1997b) differs only (Dendrocygna) are placed inside the subfamily Anserinae. by the inclusion, or not, of Dendrocygna inside this clade. This scheme has been mainly confirmed by Livezey The DNA–DNA hybridization results of Sibley and (1997b), who nevertheless proposed that Dendrocygna Ahlquist (1990) give rise to an even different scheme with represents an independent lineage, unrelated to Anseri- three, main lineages (Fig. 1C and Appendix A): (i) the Fig. 1. Schematic phylogenies of the Anseriformes according to (A) Del Hoyo et al. (1992); (B) Livezey (1997b); and (C) Sibley and Ahlquist (1990). Only the 24 genera analyzed in our study plus Anseranas are depicted in these trees. The subfamilies Anatinae and Anserinae (or the tribes Anatini and Anserini) defined by the various authors are indicated. C. Donne-Gousse et al. / Molecular Phylogenetics and Evolution 23 (2002) 339–356 341 Anatini, which has a composition different from that of verging first and then a split between Anserinae (Anser, the Anatidae of Del Hoyo et al. (1992) and Livezey Branta, and Cygnus) and Anatinae (Sorenson et al., (1997b); (ii) the Anserini, including Tadornini and Cai- 1999a). Within Anatinae four main clades were found: (i) rina; and (iii) the genera Cygnus and Coscoroba which Anas and related genera; (ii) a clade containing Tador- together form an independent grouping called Cygninae. nini (Tadorna and Chloephaga) allied with Cairina and Given the strong level of discrepancy existing between Aix (this group is then clustered with Mergini (Bucep- the three main published phylogenies at the family and hala)); (iii) Aythyini (Aythya, Netta and Marmaronetta) subfamily levels, it is not surprising that the relation- with other genera such as Cyanochen and Pteronetta; and ships inside each subfamily are also a matter of con- (iv) Chenonetta and Sarkidiornis. Despite their interest in tention (Fig. 1). As shown in Fig. 1A, Del Hoyo et al. clearly indicating that a robust phylogenetic signal exists (1992) found five main tribes in the Anatinae. Some of in mtDNA to resolve waterfowl phylogeny, most of these these tribes such as Mergini (Mergus, Bucephala, Mel- molecular analyses were based on a limited sampling of anitta, Somateria, and Clangula) were also found by species or only marginally discuss the relationships be- Livezey (1997b). The tribe called Aythyini has different tween the various groups of Anseriformes. For these compositions for the two authors since Livezey (1997b) reasons we sequenced and analyzed the mtDNA control includes Marmaronetta in this clade, whereas Del Hoyo region from 45 Anseriformes representing 24 genera. Our et al. (1992) consider it as more closely related to Anas. sampling includes representatives of all of the main tribes Other
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