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1471-2148-7-35.Pdf BMC Evolutionary Biology BioMed Central Research article Open Access Multilocus perspectives on the monophyly and phylogeny of the order Charadriiformes (Aves) Matthew G Fain and Peter Houde* Address: Department of Biology, New Mexico State University, Box 30001 MSC 3AF, Las Cruces New Mexico 88003 USA Email: Matthew G Fain - [email protected]; Peter Houde* - [email protected] * Corresponding author Published: 8 March 2007 Received: 25 September 2006 Accepted: 8 March 2007 BMC Evolutionary Biology 2007, 7:35 doi:10.1186/1471-2148-7-35 This article is available from: http://www.biomedcentral.com/1471-2148/7/35 © 2007 Fain and Houde; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: The phylogeny of shorebirds (Aves: Charadriiformes) and their putative sister groups was reconstructed using approximately 5 kilobases of data from three nuclear loci and two mitochondrial genes, and compared to that based on two other nuclear loci. Results: Charadriiformes represent a monophyletic group that consists of three monophyletic suborders Lari (i.e., Laridae [including Sternidae and Rynchopidae], Stercorariidae, Alcidae, Glareolidae, Dromadidae, and Turnicidae), Scolopaci (i.e., Scolopacidae [including Phalaropidae], Jacanidae, Rostratulidae, Thinocoridae, Pedionomidae), and Charadrii (i.e., Burhinidae, Chionididae, Charadriidae, Haematopodidae, Recurvirostridae, and presumably Ibidorhynchidae). The position of purported "gruiform" buttonquails within Charadriiformes is confirmed. Skimmers are most likely sister to terns alone, and plovers may be paraphyletic with respect to oystercatchers and stilts. The Egyptian Plover is not a member of the Glareolidae, but is instead relatively basal among Charadrii. None of the putative sisters of Charadriiformes were recovered as such. Conclusion: Hypotheses of non-monophyly and sister relationships of shorebirds are tested by multilocus analysis. The monophyly of and interfamilial relationships among shorebirds are confirmed and refined. Lineage-specific differences in evolutionary rates are more consistent across loci in shorebirds than other birds and may contribute to the congruence of locus-specific phylogenetic estimates in shorebirds. Background in general agreement as to recognition of the suborders The order Charadriiformes is one of relatively few exam- Charadrii, Scolopaci, and Lari as clades. However, mor- ples in which the phylogenetic relationships of a major phological studies also recognized the Alci as distinct higher-level clade of birds are becoming successfully [4,5], whereas DNA-DNA hybridization placed them near resolved [1,2]. The order includes what have traditionally gull-like birds in the Lari. In contrast, recent molecular been known as the shorebirds, a diverse and apparently studies sampling both nuclear and mitochondrial ancient group of non-passerine birds whose three subor- sequences have generated a remarkably consistent and ders are estimated to have diverged from one another in highly-resolved interfamilial tree for Charadriiformes the Cretaceous [3]. Earlier morphological and biochemi- [2,3,6,7]. cal analyses produced conflicting pictures of shorebird phylogeny. Morphological and biochemical studies were Page 1 of 15 (page number not for citation purposes) BMC Evolutionary Biology 2007, 7:35 http://www.biomedcentral.com/1471-2148/7/35 While the monophyly of Charadriiformes is popularly independently studied the relationships of Charadrii- accepted, it has been questioned both implicitly and formes using DNA sequences from two other nuclear loci explicitly. Olson and Feduccia hypothesized that charadri- (myoglobin chromosome 1, position 48,720.4K, and RAG- iform stilts (i.e., Recurvirostridae) were ancestral to both 1 chromosome 5, position 16,597.6K in chicken) and waterfowl (Anseriformes) and flamingos (Phoenicopteri- nearly complete mitochondrial genomes [2,3,6]. We also dae) based on their interpretation of fossils and compara- test the monophyly and sister relationships of Charadrii- tive anatomy [8-11]. Like some early anatomists of the formes by multi-locus sequence analysis including all the 19th century, Olson portrayed the "gruiform" bustards aforementioned putative ingroups or sister groups. (Otididae) as Charadriiformes, closely related to the coursers (Glareolidae) and in particular to the Egyptian Of note, no single molecular phylogenetic analysis of Plover [10]. He further advocated an ill-defined relation- Charadriiformes has yet included representatives of all its ship of ibises (Ciconiiformes: Threskiornithidae) "unit- member families. The monotypic Ibisbill (Ibidorhynchi- ing" Gruiformes and Charadriiformes [10,12]. Sibley et al. dae) has yet to be studied by anyone, although it is gener- found rails (Rallidae) to be statistically inseparable from ally presumed to fall within the Charadrii, near stilts. both Gruiformes and Charadriiformes using DNA-DNA Paton et al. [3] and Paton & Baker [2] lacked DNA hybridization [13]. sequences of Ibisbill and the monotypic Crab Plover (Dromadidae). Ericson et al. [6] lacked these as well as These hypotheses have been discredited piecemeal in buttonquails (Turnicidae) and the monotypic Australian recent years. Specifically, there exists strong evidence for Plains-wanderer (Pedionomidae). Thomas et al. the sistership of waterfowl and fowl as Galloanserae, the [23]lacked eight of the traditionally recognized charadrii- sister to Neoaves [14-16]. There is also strong evidence for form families in their study of mitochondrial cytochrome-b a clade of flamingos and grebes [17,18] within Metaves, DNA sequences. Likewise, we were unable to include Ibis- one of two hypothesized basal clades of Neoaves (the bill, Crab-Plover, sheathbills (Chionididae), and the other being Coronaves, to which shorebirds belong) genus Pluvianellus, the last of which is not a member of the [7,19]. All subsequent studies have upheld the novel family Charadriidae in which it is traditionally included transfer of both Australian Plains-wanderer (Pedionomi- [3]. Our results corroborate numerous novel family-level dae) and buttonquails (Turnicidae) from the order Grui- relationships reported in the aforementioned recent stud- formes to Charadriiformes [2,3,7,20,21]. ies, including the positions of the traditional gruiform Turnicidae basal to a clade of glareolids, larids, alcids and However, many of the proposed interrelationships of relatives (suborder Lari). In the present study, we include gruiform, charadriiform, and ciconiiform taxa have not two putative representatives of Glareolidae, the Double- yet been explicitly tested in a comprehensive molecular banded Courser (Rhinoptilus africanus) and the Egyptian phylogenetic framework with both evidence from multi- Plover (Pluvianus aegyptius). Pluvianus has not been ple independent loci and comprehensive taxon sampling. included previously in molecular analyses, and in contrast Gruiformes or sandgrouse (Pterocliformes) have been to traditional classifications, we conclude that this genus cited most commonly as potential sister groups of is distinct from the Glareolidae, with closer relations Charadriiformes and representative members of these within the Charadrii than the Lari. groups have generally been used to root a presumed monophyletic Charadriiformes. The monophyly of Last, some interfamilial relationships have not been well- Charadriiformes has been tested only with limited taxon resolved in previous single-locus nuclear or mitochon- sampling [6]; with incomplete DNA-DNA hybridization drial molecular data sets. For example, myoglobin intron 2 matrices [21]; or with single-locus studies [7]. In the proc- and RAG-1 suggested that Recurvirostridae and Haemat- ess of studying the phylogenetic relationships of Grui- opodidae may be nested within Charadriidae, rendering formes [22]we had the opportunity to characterize and the latter paraphyletic. Also unresolved is whether skim- analyze more than 5 kb of DNA sequences from four loci mers ("Rynchopidae") are sister to either gulls (Larinae) (mitochondrial and three nuclear) from a variety of puta- or terns (Sterninae) or both [2,3,6]. Further, a potential tive sister groups of Gruiformes, including multiple repre- conflict in topology exists between myo-2 and RAG-1 [6] sentatives of most families of Charadriiformes. Our novel as to whether Jacanidae is sister to Thinocoridae (seed- data include intronic and exonic sequences from beta- snipes) or to Rostratulidae (painted-snipes). The data at fibrinogen, alcohol dehydrogenase-1, and glyceraldehyde-3- hand address these relationships. phosphate dehydrogenase. These map to chromosomes 4 (position 20,917K), 4 (position 60,497K), and 1 (posi- Results tion 71,016.5K), respectively, in chicken. We present the Molecular Characterization results of phylogenetic analyses of these loci for Charadri- We sampled four independent, presumably unlinked loci iformes and compare our results to those of others, who to test recent novel hypotheses of relationships within Page 2 of 15 (page number not for citation purposes) BMC Evolutionary Biology 2007, 7:35 http://www.biomedcentral.com/1471-2148/7/35 Charadriiformes and to test monophyly of the group com- the codon positions. Model selection for the entire align- prehensively, particularly
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