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2009A (Braun and Huddleston) Copy.Pdf Molecular Phylogenetics and Evolution 53 (2009) 948–960 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev A molecular phylogenetic survey of caprimulgiform nightbirds illustrates the utility of non-coding sequences Michael J. Braun a,b,*, Christopher J. Huddleston a a Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 4210 Silver Hill Road, Suitland, MD 20746, USA b Behavior, Ecology, Evolution, and Systematics Program, University of Maryland, College Park, MD 20742, USA article info abstract Article history: The order Caprimulgiformes comprises five bird families adapted to nocturnal activity. The order has been Received 10 February 2009 regarded as monophyletic, but recent evidence suggests that swifts and hummingbirds (Apodiformes) Revised 19 August 2009 belong within it. To explore the group’s phylogeny, we obtained more than 2000 bp of DNA sequence Accepted 25 August 2009 from the cytochrome b and c-myc genes for 35 taxa, representing all major lineages and outgroups. Available online 29 August 2009 Non-coding sequences of the c-myc gene were unsaturated, readily alignable and contained numerous informative insertions and deletions (indels), signalling broad utility for higher level phylogenetics. A Keywords: 12 bp insertion in c-myc links Apodiformes with owlet-nightjars, confirming paraphyly of the traditional Phylogeny Caprimulgiformes. However, even this rare genomic change is homoplasious when all birds are consid- Evolution Caprimulgiformes ered. Monophyly of each of the five traditional families was strongly confirmed, but relationships among Aegothelidae families were poorly resolved. The tree structure argues against family status for Eurostopodus and Apodiformes Batrachostomus, which should be retained in Caprimulgidae and Podargidae, respectively. The genus Bird Caprimulgus and both subfamilies of Caprimulgidae appear to be polyphyletic. The phylogeny elucidates Systematics the evolution of adaptive traits such as nocturnality and hypothermia, but whether nocturnality evolved Insertions once or multiple times is an open question. Deletions Published by Elsevier Inc. Rare genomic changes Non-coding sequences 1. Introduction The traditional avian order Caprimulgiformes comprises about 120 species intricately adapted to nocturnal, mostly insectivorous The impact of molecular data on systematics has been dramatic. lifestyles. It includes some familiar birds, such as the nightjars Insights from molecular phylogenies have revolutionized our (Caprimulgus) and nighthawks (Chordeiles), as well as many exotic thinking about evolutionary relationships, especially in poorly and bizarre forms, such as the oilbird (Steatornis), a frugivorous, known groups. At the same time, it has become clear that short echo-locating troglodyte of South American jungles. Their noctur- DNA sequences from a single gene will not be sufficient to obtain nal nature, cryptic plumage, secretive behavior, and generally trop- stable phylogenies for many groups. Single-gene trees may differ ical distributions make most caprimulgiforms difficult to study in from each other and from the species tree under a variety of cir- life. They are consequently among the most poorly known groups cumstances (Maddison, 1997; Kubatko and Degnan, 2007), and of birds. Information concerning their taxonomy, distribution and the resolving power of a particular gene will depend on how well life history has been spotty and scattered, but several recent trea- its rate of evolution is matched to the structure of the tree in ques- tises summarize available information (Cleere, 1998, 1999; Cohn- tion (Braun and Kimball, 2002). Obtaining reliable, well-resolved Haft, 1999; Holyoak, 1999a,b; Thomas, 1999; Holyoak, 2001). phylogenies for many groups will require data from multiple genes The generally primitive state of caprimulgiform systematics is evolving at a variety of rates (Rokas and Carroll, 2005). To this end, illustrated by the continuing discovery of new genera (Cleere we here present mitochondrial and nuclear DNA sequence data for et al., 2007) and new species (Louette, 1990; Lencioni-Neto, 1994; a broad sampling of a ubiquitous but little known order of birds. Safford et al., 1995; Sangster and Rozendaal, 2004). However, con- tinued research on vocalizations and morphology further improves our understanding of nightbird species and species groups (Davis, 1962, 1978; Schulenberg et al., 1984; Fry, 1988; Cohn-Haft, 1993; * Corresponding author. Address: Department of Vertebrate Zoology, National Robbins et al., 1994; Robbins and Parker, 1997; Pratt, 2000; Cleere, Museum of Natural History, Smithsonian Institution, 4210 Silver Hill Road, Suitland, Maryland 20746, USA. Fax: +1 301 238 3059. 2002) and a number of pertinent molecular and morphological phy- E-mail address: [email protected] (M.J. Braun). logenetic studies have now been published (Sibley and Ahlquist, 1055-7903/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.ympev.2009.08.025 M.J. Braun, C.J. Huddleston / Molecular Phylogenetics and Evolution 53 (2009) 948–960 949 1990; Mariaux and Braun, 1996; Brumfield et al., 1997; Johansson is not clear whether they support monophyly of either group. Both et al., 2001; Mayr, 2002; Mayr et al., 2003; Dumbacher et al., DNA hybridization and DNA sequence data strongly suggest that 2003; Barrowclough et al., 2006; Ericson et al., 2006; Larsen et al., Eurostopodus species are sister to a clade including all other capri- 2007; Livezey and Zusi, 2007; Hackett et al., 2008). mulgids examined, and that relationships within the remaining Seminal works on caprimulgiform systematics were written by caprimulgids are inconsistent with the standard caprimulgine/ Sclater (1866a,b), Beddard (1886), Wetmore (1918), Peters (1940), chordeiline split (Sibley and Ahlquist, 1990; Mariaux and Braun, and Tripepi et al. (2006). In addition, a detailed historical review 1996; Barrowclough et al., 2006; Larsen et al., 2007). was given by Sibley and Ahlquist (1990) and updated by later A well-resolved and well-supported phylogenetic tree for authors. Key features and questions are summarized here. The or- Caprimulgiformes would provide an organizing framework with der includes five distinctive lineages, usually accorded family rank. which to understand their biology and evolutionary history. These are the nightjars and nighthawks (Caprimulgidae; 89–90 Toward that end, we here extend the cytochrome b sequence data species), frogmouths (Podargidae; 13 species), owlet-nightjars set of Mariaux and Braun (1996) to include new ingroup and out- (Aegothelidae; 9 species), potoos (Nyctibiidae; 7 species), and oil- group taxa, and add a second gene sequence from the nuclear locus bird (Steatornithidae; 1 species). Although the monophyly of each c-myc. The c-myc gene is more slowly evolving than cytochrome b, of these lineages has never been seriously questioned, Sibley and providing better resolution deep in the tree (Harshman et al., Ahlquist (1990) suggested erecting two new families based on 2003). Because it includes non-coding sequence elements that deep divergences in their DNA hybridization data: Eurostopodidae accommodate length variation more readily than protein-coding for the nightjar genus Eurostopodus, and Batrachostomidae for the sequences, c-myc also provides a relatively large number of phylo- frogmouth genus Batrachostomus. This finding is consistent with a genetically informative insertion/deletion (indel) characters. The fossil record extending back to Eocene times for several groups expanded data set provides clear evidence that the traditional or- (Mourer-Chauviré, 1982, 1987; Olson, 1987; Peters, 1991), which der Caprimulgiformes is paraphyletic, and allows us to address is as early as any modern bird families appear (James, 2005). Other several of the systematic issues mentioned above. molecular data are also consistent with these deep splits (Mariaux and Braun, 1996; Brumfield et al., 1997; Barrowclough et al., 2006; 2. Materials and methods Cleere et al., 2007; Larsen et al., 2007). Morphological diversity (Hoff, 1966) and genetic divergences 2.1. Tissue samples and data collection (Sibley and Ahlquist, 1990; Mariaux and Braun, 1996) among the five lineages are even greater than those within them. In fact, accu- Tissue samples from 34 nightbirds and putative relatives were mulated divergence is so great that several analyses of molecular obtained from our own fieldwork and from genetic resource collec- and morphological data failed to recover a close relationship among tions of major museums (Table 1). The partial cytochrome b se- the five lineages (Johansson et al., 2001; Mayr, 2002; Chubb, 2004; quences of Mariaux and Braun (1996) were confirmed and Cracraft et al., 2004; Fain and Houde, 2004; Barrowclough et al., extended to encompass the entire coding sequence. We used 2006; Ericson et al., 2006; Livezey and Zusi, 2007), leading to suspi- chicken (Gallus gallus) cytochrome b and c-myc sequences from cions that the order might be polyphyletic. These suspicions were GenBank (NC_001323 and J00889) as an unambiguous outgroup exacerbated by strong indications of a sister group relationship of for phylogenetic analyses. Genomic DNA was extracted from tis- owlet-nightjars with swifts and hummingbirds (Mayr, 2002; Mayr sues using methods described in Mariaux and Braun (1996) and et al., 2003; Cracraft et al., 2004; Barrowclough et al., 2006; Ericson Robbins et al.
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