Rhodinocichla Rosea Is an Emberizid (Aves; Passeriformes)
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MOLECULAR PHYLOGENETICS AND EVOLUTION Vol. 8, No. 2, October, pp. 260-274, 1997 ARTICLE NO. FY970426 Rhodinocichla rosea Is an Emberizid (Aves; Passeriformes) Based on Mitochondrial DNA Analyses GillesSeutin1 and Eldredge Bermingham Svithsonian Tropical Fbsearch Institute, Apartado 2072, Balboa, Panama Received September 16, 1997; revised March 25, 1997 morphology, behavior, and other phenotypic traits (e.g., The systematic position of the avian species Rhodino- Gill, 1990). However, in many other cases, the phyloge- cichla rosea is unclear. Recent opinions are that it is netic relationships of taxa are unclear, and the conver- either a mockingbird (family Mimidae) or a tanager gent nature of specific phenotypic attributes is uncer- (Thraupinae; Emberizidae). In either case, it would be tain. This is the case with the rosy thrush-tanager, an atypical member of the family. We sequenced ap- Rhodinocichla rosea. proximately 600 bases of the mitochondrial cyto- The rosy thrush-tanager is the only member of the chrome oxidase I (COI) gene of Rhodinocichla, several highly distinctive genus Rhodinocichla. It is a medium- mimids, tanagers, and other passerines. We used maxi- mum likelihood (ML), distance and parsimony ap- sized neotropical passerine (total length, 19-20 cm; proaches to analyze the sequences and concluded that weight, 43-52 g) with several geographically localized Rhodinocichla belongs to the family Emberizidae. Phe- and widely separated populations (Isler and Isler, notypic characteristics that suggested its relationship 1987). The species was described by Lesson (1832) as a with mimids are the product of convergent evolution. Furnariidae, based on superficial similarities with the The precise relationships of Rhodinocichla within the then-known members of this family of primitive song- Emberizidae could not be resolved. Short internal birds. Soon after, it was recognized as belonging to the branches in ML and distance trees suggested, as did oscines (Hartlaub, 1853), a large group of derived earlier genetic studies, that the radiation of that fam- passerines (see Fig. 1). But Rhodinocichla also proved ily was explosive. Apparently, the extent of the tana- to possess a mosaic of phenotypic characters that made gers as a higher taxon needs to be clarified. Our it difficult to assign the genus to a particular family. analysis of the evolutionary dynamics of avian COI Clark (1913), Skutch (1962), Eisenmann (1962), Clark suggested that its usefulness for phylogenetic studies (1974), and Raikow (1978) presented and discussed is limited because silent positions saturate rapidly and morphological, anatomical, myological, and behavioral replacement substitutions are rare. Thus, our data peculiarities of the species. Over the last 100 years, the indicate that COI nucleotide data will be most useful in thrush-tanager has been classified with the wrens intraspecinc investigations, while other data sug- (Troglodytidae), the wood-warblers (Parulinae; Emberi- gested its usefulness at the interordinal level. © 1997 zidae), and, most frequently, the mockingbirds (Mimi- Academic Press dae) or the tanagers (Thraupinae; Emberizidae) (e.g., Sharpe, 1881; Ridgway, 1902; Hellmayr, 1936; Eisen- mann, 1962; Skutch, 1962; A.O.U., 1983; Webster, INTRODUCTION 1988). These various families and subfamilies are not Cases of convergent evolution demonstrate how alter- closely related in either traditional classifications (e.g., native evolutionary pathways can lead to a single Wetmore, 1960; A.O.U., 1983) or that presented by phenotypic solution and help identify constraints limit- Sibley and Ahlquist (1990; Fig. 1). For instance, if one ing the evolution of phenotypes. But convergent evolu- accepts Sibley and Ahlquist's (1990) estimates and tion, because it produces similarities between organ- calibration of single copy nuclear DNA divergence, the isms not resulting from common ancestry, can mask the mimids and the tanagers last shared a common ances- genealogical relationships of taxa. In birds, there are tor 20-30 MY ago. This date for a mimid-tanager split several well-documented examples of convergence in conforms to fossil evidence suggesting that most oscine families were probably established well before the end of the Miocene (Brodkorb, 1971; Feduccia, 1980; Olson, 1 Present address: Department of Geography, McGill University, 1985). 805 Sherbrooke West, Montreal, Quebec, Canada H3A 2K6. Fax: The essential problem with previous discussions of (514) 398-7437; E-mail: [email protected]. the taxonomic affinities of Rhodinocichla was that the 260 1055-7903/97 $25.00 Copyright © 1997 by Academic Press All rights of reproduction in any form reserved. Rhodinocichla IS AN EMBERIZID 261 Suboscines (incl. Furnariidae) enigmas (Edwards et al., 1991; Aviso et al., 1994a; Zimmer et al., 1994; but see Aviso et al., 1994b). We Corvida (incl. Vireonidae) investigated the phylogenetic relationships of Rhodino- cichla by analyzing roughly 600 base pairs (bp) of the Mimidae gene coding for the first subunit of the cytochrome c oxidase protein (COI or Coxl). The analyses strongly Turdinae indicate that Rhodinocichla is a tanager, not a mimid. The data also allowed us to investigate the evolution- ary dynamics of avian COI and its general utility for Troglodytidae phylogenetic studies of birds. Parulinae MATERIALS AND METHODS New World nine-primaried Cardinalinae oscines Samples. Our samples (Table 1, see also Fig. 1) (Emberizidae) included Rhodinocichla rosea, one species each repre- Thraupinae senting Troglodytidae, Turdinae, Parulinae, and Cardin- alinae, and three species each of Mimidae and Thraupi- FIG. 1. Relationships of passerine groups following Sibley and nae. For most species, we sequenced two individuals, Ahlquist (1990). Only those groups relevant to the discussion of and in all but one case we surveyed two or more Rhodinocichla affinities are shown. Family and subfamily names follow A.O.U. (1983). members of a subfamily (range 2-5). Further, we included two species of Vireonidae as outgroups. Until recently, Vireonidae were thought to be nine-primaried characters considered were often not analyzed in an oscines (e.g., A.O.U., 1983), but they are now known to appropriate context. First, the homologous nature of be part of the corvine radiation (Johnson et al., 1988; several shared traits used to infer relationships had not Sibley and Ahlquist, 1990). Thus, vireos were an appro- been ascertained. Second, character similarities be- priate outgroup for our analyses (Fig. 1). Most tissue tween taxa were typically taken as evidence of relation- samples were collected as biopsies from live birds and ships, even though no consideration was given to preserved in a salt-DMSO solution (Seutin et al., 1991, whether the traits were ancestral or derived. A defini- 1994); other samples came from sacrificed individuals tive taxonomic assignment of Rhodinocichla, indepen- (see Appendix). DNA was extracted from small pieces of dent of phenotypic characters, should help us to under- pectoral muscle (average 0.05 g) using phenol-chloro- stand the evolution of its numerous anatomical and form extractions described by Seutin et al. (1993). behavioral peculiarities. PCR amplifications and sequencing. A DNA se- Mitochondrial DNA (mtDNA) sequence data have quence of 681 base pairs (bp), corresponding to approxi- been fruitfully utilized to resolve avian taxonomic mately 45% of the COI gene, was amplified by the TABLE 1 Samples Analyzed in the Study of the Relationships of Rhodinocichla rosea No. of differences between Species Family or subfamily samples; TS + TV Location Troglodytes aedon Troglodytidae 1 na° Dominica, West Indies Turdus nudigenis Turdinae 2 0 + 0 Martinique, West Indies (Muscicapidae) St. Lucia, West Indies Mimus longicaudatus Mimidae 1 na Peru Toxostoma rufum Mimidae 1 na Louisiana; U.S.A. Cinclocerthia rufi.ca.uda Mimidae 2 5 + 0 Dominica, West Indies St. Vincent, West Indies Vireo flavoviridis Vireonidae 2 3 + 1 Prov. de Panama; Panama Vireo altiloquus Vireonidae 2 0 + 0 Dominica, West Indies Dendroica adelaidae Parulinae 2 0 + 0 St. Lucia, West Indies Tangara inornata Thraupinae 2 0 + 0 Prov. de Colon; Panama Thraupis episcopus Thraupinae 1 na Estado de Sucre; Venezuela Ramphocelus carbo Thraupinae 2 0 + 0 Estado de Sucre; Venezuela Rhodinocichla rosea 2 0 + 0 Prov. de Panama; Panama Saltator albicollis Cardinalinae 1 na St. Lucia, West Indies Note. Taxonomic sequence and nomenclature follow A.O.U. (1983). " na: not applicable. 262 SEUTIN AND BERMINGHAM polymerase chain reaction (PCR) using primers COIa variation in nucleotide usage, we calculated the coeffi- and COIf described by Palumbi et al. (1991). Amplifica- cient of variation (CV) of the proportion of each base in tions were carried on for 25 cycles with Perkin-Elmer the different sequences for each of the three codon AmpliTaq DNA polymerase. In each cycle, samples positions. CV of the four nucleotides at a codon position were denatured at 94°C for 45 s, annealing was at 55°C were then averaged to quantify overall intersequence for 45 s, and extension was at 72°C for 60 s. Cycling was variability by position. preceded by DNA denaturation at 94°C for 3 min and To assess whether groups of sequences shared dis- was followed by a 5-min extension at 72°C. Amplifica- tinct compositional biases, we used both the GC-tree tion products were eluted in water from low-melting method proposed by Lockhart et al. (1994) and a point agarose gels using the GeneClean procedure. principal component