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This Article Appeared in a Journal Published by Elsevier. the Attached Copy Is Furnished to the Author for Internal Non-Commerci This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Molecular Phylogenetics and Evolution 55 (2010) 443–453 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev A multi-gene estimate of phylogeny in the nightjars and nighthawks (Caprimulgidae) Kin-Lan Han a,b,c,*, Mark B. Robbins d, Michael J. Braun a,b 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 20740, USA c Department of Biology, University of Florida, Gainesville, FL 32611, USA d Division of Ornithology, University of Kansas Natural History Museum and Biodiversity Institute, 1345 Jayhawk Boulevard, Dyche Hall, Lawrence, KS 66045-7562, USA article info abstract Article history: Caprimulgidae is a cosmopolitan family of nocturnal and crepuscular insectivorous birds comprising the Received 29 April 2009 nightjars, nighthawks, and relatives. Sexual selection and convergence or parallelism in plumage and Revised 16 January 2010 behavior have made it difficult to discern evolutionary relationships in this group. In order to provide Accepted 20 January 2010 a framework for comparative studies of this family, a molecular phylogeny was reconstructed using mito- Available online 1 February 2010 chondrial cytochrome b, and nuclear c-myc and growth hormone DNA sequences. Likelihood, parsimony and Bayesian analyses agree in placing Eurostopodus species and Caprimulgus enarratus, a Malagasy ende- Keywords: mic, as the earliest branches of the tree. The remaining taxa are divided among four well-supported Caprimulgidae clades, three in the New World and one in the Old World. Insertion/deletion events, common in non-cod- Nightjars Nighthawks ing sequences, provide additional support in resolving the phylogeny. Neither of the traditional subfam- Molecular phylogeny ilies, Caprimulginae (nightjars) and Chordeilinae (nighthawks), is monophyletic, suggesting that the Cytochrome b morphological specializations characterizing ‘‘nighthawks” evolved multiple times and the ‘‘nightjar” c-myc body plan is an old and conservative one. The large genus Caprimulgus is polyphyletic with respect to Growth hormone many other genera in the family, which are often defined by derived plumage traits that likely reflect sex- Convergence ual selection or ecological specialization. A taxonomic revision of the family is proposed based on the Sexual selection combined tree, including naming a new genus for C. enarratus. Evolution Ó 2010 Elsevier Inc. All rights reserved. Indels Non-coding DNA 1. Introduction leading. Nevertheless, molecular studies (Sibley and Ahlquist, 1990; Mariaux and Braun, 1996; Barrowclough et al., 2006; Lar- Convergent evolution occurs when unrelated organisms devel- sen et al., 2007; Braun and Huddleston, 2009) have begun to un- op similarities due to similar environmental or other evolution- ravel the phylogeny of this family and shed light on these ary pressures. Such similarities may be mistaken for phenomena. homologies, obscuring phylogeny. Molecular phylogenetic meth- Caprimulgidae, with approximately 90 species, is the largest of ods provide increasing evidence of convergent evolution in mor- five nocturnally adapted families in the traditional order Capri- phological adaptations. The cosmopolitan Caprimulgidae, a family mulgiformes (although the traditional order is paraphyletic; see of nocturnal or crepuscular birds (Cleere 1999), provides an Braun and Huddleston, 2009 for a recent discussion). Caprimulgi- excellent example. Due to their cryptic coloration, conserved dae has traditionally been divided into two subfamilies: Caprimul- appearance and poorly known behavior, traditional phylogenetic ginae (nightjars) and Chordeilinae (nighthawks) (Oberholser, studies based on morphology and behavior have yet to resolve 1914; Peters, 1940; Cleere, 1998, 1999; Holyoak, 2001). The cos- many systematic issues within this family (Cleere, 1998, 1999; mopolitan Caprimulginae are generally characterized by a schizog- Holyoak, 2001). This is not unexpected in a group such as Capri- nathous palate, long rictal bristles around the gape, and relatively mulgidae, since morphological and behavioral characters may be short, rounded wings. They are crepuscular or nocturnal, and often subject to uniform selection for crypticity in many taxa, creating forage by sallying after flying insects from the ground or exposed the potential for convergent or parallel evolution that can be mis- perches. In contrast, the Chordeilinae are restricted to the New World, have a desmognathous palate (but see Bühler, 1970), gener- ally lack rictal bristles, have relatively longer, narrower wings, and * Corresponding author. Department of Biology, University of Florida, P.O. Box 118525, Gainesville, FL 32611-8525, USA. are diurnal or crepuscular aerial hawkers (Oberholser, 1914; Cle- E-mail address: hankin@ufl.edu (K.-L. Han). ere, 1998, 1999; Holyoak, 2001). 1055-7903/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2010.01.023 Author's personal copy 444 K.-L. Han et al. / Molecular Phylogenetics and Evolution 55 (2010) 443–453 Sixteen genera are currently recognized (Dickinson 2003), rimulgidae and relatives. MYC included part of intron b, all of exon although as many as 51 genera have been named in the past (Pe- 3, and part of the 30 UTR. MYC is a well-studied, slowly evolving ters, 1940; Cleere, 1998, 1999). Four genera are traditionally placed proto-oncogene that is useful for studying deep divergences in ver- within Chordeilinae (Chordeiles, Lurocalis, Nyctiprogne, and Podag- tebrates (Braun et al., 1985; Graybeal, 1994; Ericson et al., 2000; er), whereas the other 12 genera (Eurostopodus, Veles, Nyctidromus, Miyamoto et al., 2000; Harshman et al., 2003). Phalaenoptilus, Siphonorhis, Nyctiphrynus, Caprimulgus, Macrodip- We asked two major questions regarding caprimulgid evolu- teryx, Hydropsalis, Uropsalis, Macropsalis, and Eleothreptus) are usu- tion: (1) Are the large genera Caprimulgus (55–57 species) and ally placed within Caprimulginae. The composition of the two Eurostopodus (seven species) monophyletic? Non-monophyly subfamilies, however, remains debatable, and molecular data sug- could suggest that these birds have maintained a successful life- gest that one or both may not be monophyletic (Sibley and Ahl- style and body plan while morphologically divergent forms arose quist, 1990; Mariaux and Braun, 1996; Barrowclough et al., 2006; from within the group through adaptation or sexual selection. (2) Braun and Huddleston, 2009). In the most recent monograph of Are the two subfamilies, Chordeilinae and Caprimulginae, mono- Caprimulgiformes, Holyoak (2001) placed Podager in Caprimulgi- phyletic? If both subfamilies are monophyletic, then aerial hawk- nae because of the presence of rictal bristles, which are lacking ing and sallying, and the morphological adaptations associated in other chordeilines. Eurostopodus and Veles (=Caprimulgus binota- with each foraging mode, may have each evolved only once in tus) were moved to Chordeilinae because they lack rictal bristles. the family. If neither subfamily is monophyletic, then one or both The presence or absence of rictal bristles requires further study be- of these suites of behavioral and morphological adaptations must cause they are much reduced or vestigial in some taxa (KLH, pers. have arisen multiple times through convergent or parallel obs.). Eurostopodus shares other morphological affinities with evolution. Chordeilinae such as a square tail and narrow, pointed wings (Schodde and Mason, 1980; Holyoak, 2001). 2. Materials and methods Based on plumage, Eurostopodus has even been subsumed with- in Caprimulgus (e.g., Schodde and Mason, 1980), but molecular evi- 2.1. Taxon sampling dence has consistently shown Eurostopodus to be genetically divergent from all other caprimulgids (Sibley and Ahlquist, 1990; We follow the taxonomy of Dickinson (2003) as the most recent Mariaux and Braun, 1996; Barrowclough et al., 2006; Larsen comprehensive treatment of the family. Samples from 66 capri- et al., 2007; Braun and Huddleston, 2009). Sibley and Ahlquist mulgid specimens were included in the study (Appendix A) repre- (1990) suggested that Eurostopodus should be given family status, senting 55 of 89 caprimulgid species and 14 of the 16 genera. Six and Dickinson (2003) recognized the subfamily Eurostopodinae. additional specimens from four other caprimulgiform families With increased taxon sampling, Braun and Huddleston (2009) dis- were included as outgroups. covered a deep genetic divergence within Eurostopodus, and the possibility that the genus is not monophyletic. In fact, two of the seven species, E. macrotis
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