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A Gondwanan Origin of Passerine Birds Supported by DNA Sequences of the Endemic New Zealand Wrens Per G

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A Gondwanan Origin of Passerine Birds Supported by DNA Sequences of the Endemic New Zealand Wrens Per G Received 2 July 2001 Accepted 27 September 2001 Published online 22 January 2002 A Gondwanan origin of passerine birds supported by DNA sequences of the endemic New Zealand wrens Per G. P. Ericson1*, Les Christidis2, Alan Cooper3, Martin Irestedt1,4, Jennifer Jackson3, Ulf S. Johansson1,4 and Janette A. Norman2 1Department of Vertebrate Zoology and Molecular Systematics Laboratory, Swedish Museum of Natural History, P.O. Box 50007, SE-104 05 Stockholm, Sweden 2Department of Sciences, Museum Victoria, GPO Box 666E, Melbourne, Victoria 3001, Australia 3Department of Zoology, University of Oxford, Oxford OX1 3PS, UK 4Department of Zoology, University of Stockholm, SE-106 91 Stockholm, Sweden Zoogeographic, palaeontological and biochemical data support a Southern Hemisphere origin for passerine birds, while accumulating molecular data suggest that most extant avian orders originated in the mid- Late Cretaceous. We obtained DNA sequence data from the nuclear c-myc and RAG-1 genes of the major passerine groups and here we demonstrate that the endemic New Zealand wrens (Acanthisittidae) are the sister taxon to all other extant passerines, supporting a Gondwanan origin and early radiation of passerines. We propose that (i) the acanthisittids were isolated when New Zealand separated from Gondwana (ca. 82–85 Myr ago), (ii) suboscines, in turn, were derived from an ancestral lineage that inhabited western Gondwana, and (iii) the ancestors of the oscines (songbirds) were subsequently isolated by the separation of Australia from Antarctica. The later spread of passerines into the Northern Hemisphere reflects the northward migration of these former Gondwanan elements. Keywords: biogeography; Gondwana; New Zealand wrens; Passeriformes; phylogenetic analysis; avian systematics 1. INTRODUCTION Suboscine birds are currently most numerous in South and Central America (a few genera have spread to North The New Zealand wrens are an enigmatic group of passer- America, probably after the formation of the Panama ines (Raikow 1982), which appear intermediate between isthmus (ca. 3–5 Myr ago)) and also inhabit tropical areas the oscines and suboscines, the two major groups of of southeast Asia, Madagascar and Africa. The New passerine birds (Mu¨ller 1847). The two extant taxa World and Old World groups of suboscines are monophy- (rifleman, Acanthisitta chloris and rock wren, Xenicus letic sister lineages (Sibley & Ahlquist 1990; Irestedt et gilviventris) are remnants of an endemic radiation that al. 2001). included at least seven taxa, several of which are assumed The oscine passerines have been divided by DNA–DNA to have been flightless (Sibley et al. 1982; Millener 1988). hybridization data into the major groups Corvida and Pas- Ancient DNA studies indicate that the extant and recently serida (Sibley & Ahlquist 1990), with the former centred extinct members are genetically close, possibly as the in Australasia and the latter in the Old World and North result of a bottleneck during a marine transgression in the America. The monophyly of the Passerida is supported by Oligocene period (Cooper 1994; Cooper & Cooper 1995). a synapomorphic insertion of one amino acid in the The oscines and suboscines can be separated, in cladis- nuclear c-myc gene sequence (Ericson et al. 2000), while tic terms, by the derived, complex anatomy of the syrinx the monophyly of Corvida remains to be verified by inde- in oscines (Forbes 1882; Ames 1971) and the unique, bul- pendent data. bous columella in suboscines (Feduccia 1975). The New DNA–DNA hybridization data (Sibley & Ahlquist Zealand wrens cannot be allocated to either group, as they 1990) also suggest that the Corvida comprises three super- possess the primitive states for both of these characters. families of which Menuroidea is basal to Meliphagoidea Myological data support an oscine affinity on the basis of and Corvoidea. The first two superfamilies only inhabit a single character: the shared loss of the distal belly of one the Australo–Papuan region, while several members of the flexor muscle in the leg (Raikow 1987). Although DNA– Corvoidea have dispersed from this region to radiate out DNA hybridization data indicate a sister-group relation- into other parts of the world (e.g. crows and jays, ship between New Zealand wrens and the suboscines drongos, shrikes). (Sibley & Ahlquist 1990), this is not consistent with egg- The Passerida is traditionally considered to include two white protein data (Sibley 1970). Recently, nuclear c-mos major oscine radiations, the ‘Old World insect eaters and sequence studies failed to clarify the relationships between their relatives’ and ‘New World insect eaters and finches’ oscines, suboscines and New Zealand wrens (Lovette & (Mayr & Greenway 1956; Voous 1985), of which the lat- Bermingham 2000). ter roughly corresponds to the superfamily Passeroidea (sensu Sibley & Ahlquist 1990). Within Passeroidea, the * Author for correspondence ([email protected]). two most speciose families are the Emberizidae, centred Proc. R. Soc. Lond. B (2002) 269, 235–241 235 2002 The Royal Society DOI 10.1098/rspb.2001.1877 236 P. G. P. Ericson and others Gondwanan origin of passerine birds 99/98 Pipra 92/91 97 Muscivora suboscines oscines 90 100/100 Furnarius 99/98 100 Lepidocolaptes 99 Pitta 99/98 83/84 100 Smithornis 63/64 80 Philepitta 82 68/64 Menura Menuroidea 61 Climacteris Menuroidea Corvida Passerida 99/98 99/99 Malurus Meliphagoidea 98 100 Ptiloprora Meliphagoidea 67/73 57/53 93/92 Corcorax Corvoidea 62 86 Epimachus Corvoidea 57/74 Zosterops 53 90/89 100/99 Mimus 89 86/88 99 Sturnus 82 Passer 95/95 Agelaius 99 79/79 50/52 67 Coccothraustes 76 Loxia Acanthisitta out-groups Figure 1. Phylogenetic relationships among major groups of passerine birds based on 1407 bp of nucleotide sequence data derived from two nuclear protein-coding genes, using 21 non-passerine taxa as out-groups. The tree shown is the ML tree, and is identical to one of the two most parsimonious trees found. The other most parsimonious tree differs only in the interrelationships of Agelaius, Coccothraustes and Loxia. The tree topology is similar to that based on DNA–DNA hybridization distances (Sibley & Ahlquist 1990), except for the basal position of the New Zealand wrens and the paraphyly of the Corvida relative to the Passerida. Branch lengths are proportional to the estimated genetic distances. Bootstrap values are given above branches for the MP analyses (1000 replicates); dataset with many non-passerine out-groups (left) and with Amazonetta, Corythaixoides, Cuculus, Gallus, Heliomaster, Momotus and Picumnus as out-groups (right). Bootstrap values for the ML analysis (1000 replicates) for the latter dataset are shown below the branches. in the New World, and the Fringillidae, primarily distrib- (AY037838, AY037845), Dendrocolaptidae: Lepidocolaptes uted in the Old World. The emberizids and fringillids are angustirostris (NRM 937184, AF295168, AF295190), Furnarii- considered to be sister taxa. dae: Furnarius cristatus (NRM 966772, AF295165, AF295187), A vicariant origin for the passerines has been proposed Tyrannidae: Muscivora tyrannus (NRM 976722, AF295182, from biogeographic and phylogenetic data, based on the AF295203), Pipridae: Pipra fasciicauda (NRM 947271, break up of the Cretaceous super-continent Gondwana AF295175, AF295196), Pittidae: Pitta angolensis (ZMCU (Cracraft 1973, 2001). This is supported by recent mol- S1027, AF295176, AF295197), Eurylaimidae: Smithornis rufola- ecular evidence, which suggests that extant avian orders teralis (FMNH 391675, AF295179, AF295200), Philepittidae: diverged in the Early–Mid Cretaceous (Sibley & Ahlquist Philepitta castanea (ZMCU S458, AF295172, AF295193), Men- 1990; Hedges et al. 1996; Cooper & Penny 1997; Cooper uridae: Menura novaehollandiae (AM LAB1112, AF295169, et al. 2001; Van Tuinen & Hedges 2001). In contrast, a AF295191), Climacteridae: Climacteris rufa (MV 155, literal interpretation of the palaeontological record has AY037839, AY037846), Maluridae: Malurus amabilis (MV been used to support a Tertiary origin for all modern avian C803, AY037840, AY037847), Meliphagidae: Ptiloprora plum- orders (Feduccia 1996). bea (MV C173, AY037841, AY037848), Corcoracidae: Corco- To investigate these issues, we sequenced 1428 bp rax melanoramphos (AM LAB1059, AY037842, AY037849), (1407 bp aligned sequence) of two protein-coding nuclear Paradisaeidae: Epimachus albertsii (MV C148, AF377278, genes; the proto-oncogene c-myc (498 bp) and the AY037850), Zosteropidae: Zosterops nigrorum (ZMCU O2663, recombination-activating gene RAG-1 (930 bp), for the AY037843, AY037851), Mimidae: Mimus saturinus (NRM rifleman (A. chloris) and a selection of passerine and non- 966912, AF377265, AY037852), Sturnidae: Sturnus vulgarus passerine birds. Parsimony and maximum-likelihood (NRM 966615, AF377264, AY037853), Passeridae: Passer mon- (ML) analyses were used to analyse the phylogenetic tanus (NRM 976359, AF295171, AF143738), Icteridae: Age- relationships within the major groups of passerines and laius cyanopus (NRM 966916, AF377253, AY037854), the relationships with Gondwanan biogeographic events. Fringillidae: Coccothraustes coccothraustes (NRM 976374, AY037844, AY037855) and Loxia curvirostra (NRM 976546, AF377257, AY037856). Abbreviations: AM, Australian 2. MATERIAL AND METHODS Museum, Sydney; FMNH, Field Museum of Natural History, The sequences of the following in-group taxa were Chicago; MV, Museum Victoria, Melbourne; NRM, Swedish analysed (sample identification and GenBank accession num-
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