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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 FirstCite Accepted 27 September 2001 e-publishing Published online 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 01pb0487.1 2002 The Royal Society DOI 10.1098/rspb.2001.1877 01pb0487.2 P. G. P. Ericson and others Gondwanan origin of passerine birds in the New World, and the Fringillidae, primarily distrib- it is commonly believed to be found among the group of taxa uted in the Old World. The emberizids and fringillids are referred to as the Anomalogonatae (Johansson et al. 2001). considered to be sister taxa. Twenty-one species, representing 16 out of 28 families in this A vicariant origin for the passerines has been proposed assemblage, were included in the analyses: Apodidae: Apus apus; from biogeographic and phylogenetic data, based on the Bucconidae: Bucco capensis; Caprimulgidae: Eurostopodus mac- break up of the Cretaceous super-continent Gondwana rotis, Podager nacunda; Coraciidae: Coracias caudata; Cuculidae: (Cracraft 1973, 2001). This is supported by recent mol- Cuculus canorus; Galbulidae: Galbula cyanescens; Hemiprocnidae: ecular evidence, which suggests that extant avian orders Hemiprocne longipennis; Momotidae: Momotus momota; Muso- diverged in the Early–Mid Cretaceous (Sibley & Ahlquist phagidae: Corythaixoides leucogaster; Nyctibiidae: Nyctibius 1990; Hedges et al. 1996; Cooper & Penny 1997; Cooper aethereus; Picidae: Dendrocopos major, Picumnus cirratus; Podargi- et al. 2001; Van Tuinen & Hedges 2001). In contrast, a dae: Podargus strigoides; Steatornithidae: Steatornis caripensis; literal interpretation of the palaeontological record has Strigidae: Asio flammeus, Glaucidium brasilianum; Trochilidae: been used to support a Tertiary origin for all modern avian Heliomaster furcifer, Hylocharis chrysura, Phaethornis pretrei; and orders (Feduccia 1996). Trogonidae: Harpactes diardii. Trees were rooted with two galli- To investigate these issues, we sequenced 1428 bp form species (Megapodiidae: Alectura lathami; Phasianidae: (1407 bp aligned sequence) of two protein-coding nuclear Gallus gallus) and one anseriform species (Anatidae: Amazonetta genes; the proto-oncogene c-myc (498 bp) and the brasiliensis, AF427042, AY034411), as these two orders are recombination-activating gene RAG-1 (930 bp), for the thought to constitute the sister group to all other neognathous rifleman (A. chloris) and a selection of passerine and non- birds (Groth & Barrowclough 1999; Van Tuinen et al. 2000). passerine birds. Parsimony and maximum-likelihood All non-passerine sequences, except for the anatid, are already (ML) analyses were used to analyse the phylogenetic published (Irestedt et al. 2001; Johansson et al. 2001) and relationships within the major groups of passerines and deposited in GenBank. the relationships with Gondwanan biogeographic events. Laboratory procedures for the extraction of DNA, PCR amplification, and sequencing of the protein-coding nuclear genes c-myc and RAG-1 are described elsewhere (Ericson et al. 2. MATERIAL AND METHODS 2000; Irestedt et al. 2001). The sequences of the following in-group taxa were The data were analysed using maximum parsimony (MP) and analysed (sample identification and GenBank accession num- ML criteria using Paup∗ 4.0b8 (Swofford 1998). Genetic dis- bers in parentheses): Acanthisittidae: Acanthisitta chloris tances (uncorrected p-distances) were calculated using the com- (AY037838, AY037845), Dendrocolaptidae: Lepidocolaptes bined dataset of 1407 bp. Unweighted MP analyses were angustirostris (NRM 937184, AF295168, AF295190), Furnarii- performed using tree bisection–reconnection (TBR) branch dae: Furnarius cristatus (NRM 966772, AF295165, AF295187), swapping and the heuristic search option with 10 random Tyrannidae: Muscivora tyrannus (NRM 976722, AF295182, additions of taxa. ML trees were also found using TBR branch AF295203), Pipridae: Pipra fasciicauda (NRM 947271, swapping and the heuristic search option but with estimates of AF295175, AF295196), Pittidae: Pitta angolensis (ZMCU nucleotide substitutions, invariant sites and gamma parameters S1027, AF295176, AF295197), Eurylaimidae: Smithornis rufola- initially calculated from a neighbour-joining (NJ) tree. The gen- teralis (FMNH 391675, AF295179, AF295200), Philepittidae: eral time reversible (GTR) model of nucleotide substitutions Philepitta castanea (ZMCU S458, AF295172, AF295193), Men- was applied with a discrete gamma model (four rate categories) uridae: Menura novaehollandiae (AM LAB1112, AF295169, and estimates of the number of invariable sites, while alternative AF295191), Climacteridae: Climacteris rufa (MV 155, tree topologies were statistically tested using
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