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Reconstructing the Tempo and Mode of Evolution in an Extinct Clade of Birds with Ancient DNA: the Giant Moas of New Zealand

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Reconstructing the Tempo and Mode of Evolution in an Extinct Clade of Birds with Ancient DNA: the Giant Moas of New Zealand Reconstructing the tempo and mode of evolution in an extinct clade of birds with ancient DNA: The giant moas of New Zealand Allan J. Baker*†‡, Leon J. Huynen§, Oliver Haddrath*†, Craig D. Millar¶, and David M. Lambert§ *Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, ON, Canada M5S 2C6; †Department of Zoology, University of Toronto, Toronto, ON, Canada M5S 1A1; §Allan Wilson Centre for Molecular Ecology and Evolution, Institute of Molecular BioSciences, Massey University, Private Bag 102904, Auckland, New Zealand; and ¶Allan Wilson Centre for Molecular Ecology and Evolution, School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand Edited by Svante Pa¨a¨ bo, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany, and approved April 4, 2005 (received for review December 17, 2004) The tempo and mode of evolution of the extinct giant moas of New subfossil bones. Finally, the large number of moa subfossil Zealand remain obscure because the number of lineages and their remains provides the necessary material for a large-scale study divergence times cannot be estimated reliably by using fossil bone of this now-extinct group. characters only. We therefore extracted ancient DNA from 125 Although of general interest in evolutionary biology, the moa specimens and genetically typed them for a 658-bp mtDNA control radiation is less well understood than some more renowned region sequence. The sequences detected 14 monophyletic lin- passerine examples, perhaps because these birds were extinct Ϸ eages, 9 of which correspond to currently recognized species. One 100 years after human colonization of New Zealand in about of the newly detected lineages was a genetically divergent form of A.D. 1300 (7). Consequently, they are known largely from the remains recovered from caves, swamps, and middens (sites of Megalapteryx originally described as a separate species, two more discarded human food). Additionally, the complex nature of were lineages of Pachyornis in southern and northeastern New morphological variation has increased the difficulty of distin- Zealand, and two were basal lineages of South Island Dinornis. guishing within-species variation from species-level differences, When results from genetic typing and previous molecular sexing and thus moa taxonomy has been notoriously unstable. At least were combined, at least 33.6% of the specimens were incorrectly 64 species and 20 genera of moa have been named. The number classified. We used longer sequences of the control region and nine of species was reduced in successive taxonomic treatments to 20 other mtDNA genes totaling 2,814 base pairs to derive a strongly (8), 29 (9), and 13 species (1). Recent systematic revisions (cited supported phylogeny of the 14 moa lineages. Molecular dating in ref. 10) list 11 species in six genera (Megalapteryx, Dinornis, estimated the most recent common ancestor of moas existed after Pachyornis, Emeus, Euryapteryx, and Anomalopteryx), but at least the Oligocene drowning of New Zealand. However, a cycle of one of these previously described species is invalid because it lineage-splitting occurred Ϸ4–10 million years ago, when the harbors a mixture of large females and small males from two landmass was fragmented by tectonic and mountain-building species (3, 11). Whatever the precise number of species was, moa events and general cooling of the climate. These events resulted in were clearly a speciose group and outnumbered the other ratite the geographic isolation of lineages and ecological specialization. groups in species diversity. The spectacular radiation of moa lineages involved significant To investigate the tempo and mode of evolution in this extinct changes in body size, shape, and mass and provides another clade of birds, we used ancient mtDNA control region sequences to genetically type a large number of subfossil bones from example of the general influence of large-scale paleoenvironmen- museum collections in New Zealand. Using exemplars to rep- tal changes on vertebrate evolutionary history. resent the resulting control region lineages, we subsequently EVOLUTION obtained partial sequences from nine additional mtDNA genes. adaptive radiation ͉ extinct moas ͉ environmental changes These concatenated sequences were used to construct a detailed phylogeny of moa, together with appropriate outgroups. Dates eologically young island archipelagos such as the Gala´pagos of divergence were inferred from the well supported molecular GIslands and Hawaii are renowned for their relatively recent phylogeny, thus providing the first estimates of the timing of the passerine adaptive radiations, from which the classical allopatric moa radiation. Finally, we examined the tempo and mode of moa mode and tempo of evolution have been inferred. In contrast, the evolution in relation to large-scale paleoenvironmental events, radiation of the New Zealand moa could potentially be much the changing dynamics of the New Zealand landmass, and the more ancient, because the landmass broke from Antarctica͞ distribution of moa lineages through time. Ϸ Australia 80 million years ago (mya). An analysis of lineage Materials and Methods diversification in the flightless moa may reveal a contrasting DNA Extraction, PCR, and Sequencing. Because previous studies picture to that provided by the classic examples, with the have relied on specimens, including many known only from possibility of deep cladogenesis as well as more recent lineage- splitting in different geographic regions. From both a morphological and ecological perspective, moa This paper was submitted directly (Track II) to the PNAS office. represent an ideal group to investigate the tempo and mode of Abbreviations: CI, confidence interval; mya, million years ago; myr, million years. evolution. First, ratites are thought to be basal in birds, and moa Data deposition: The sequences reported in this paper have been deposited in the GenBank represent an ancient ratite group. Second, moa are remarkable database (accession nos. AY299860, AY299862–AY299864, AY299866, AY299867, because, in addition to the changes in bill morphology, they also AY299869, AY299870, AY299872, AY299873–AY299877, AY299881–AY299885, AY299888, underwent substantial changes in body size and proportions AY299891, AY299895, AY299899–AY299901, AY299903, AY299904, AY299906– AY299908, AY199912, AY299914, AY299916, AY299920, AY299922–AY299930, AY299934, (1–3). Third, it has been argued that these changes were adaptive AY299935, AY299938–AY299941, AY299943, AY299944, AY299948, AY299951, responses to the utilization of different habitats within the New AY299954–AY299957, AY299969, AY299971, DQ023671–DQ023695, DQ029126– Zealand landscape (4). Fourth, in previous studies we showed DQ029193, and DQ055458–DQ055728). that single-copy nuclear genes (3), in addition to mtDNA ‡To whom correspondence should be addressed. E-mail: [email protected]. sequences of moa (3, 5, 6), can be regularly amplified from moa © 2005 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0409435102 PNAS ͉ June 7, 2005 ͉ vol. 102 ͉ no. 23 ͉ 8257–8262 Downloaded by guest on September 29, 2021 isolated bones, incomplete specimens, or possibly mosaics of one for the 125 control region sequences (658 base pairs) and for or more species, we confined our DNA extractions to bone concatenated sequences of the control region and nine mtDNA samples catalogued as being from different specimens in New genes (ATPase 6 and 8, cyt b, ND3, ND4, ND5, COIII, 12S Zealand museum collections (see Table 2, which is published as rRNA, and tRNALys totalling 2,814 base pairs) from 40 exem- supporting information on the PNAS web site). From over 230 plars of the major moa lineages. To check the location of the root samples kindly made available to us, we were successful in of the tree, we constructed another phylogeny by using only the obtaining amplifiable DNA from 125 individuals. These samples latter nine genes, because the control region of moa could not represent all currently known moa taxa. DNA was amplified and be aligned to that of outgroup ratite and tinamou taxa (Struthio sequenced in laboratories in both Canada (Royal Ontario Mu- camelus, Casuarius casuarius, Dromaius novaehollandiae, Apteryx seum) and New Zealand (Allan Wilson Centre for Molecular haasti, and Eudromia elegans). Analyses were conducted with Ecology and Evolution, Massey University). For a listing of the MRBAYES 3.0b4 (15), and in the exemplar data set, each gene was moa samples used, the regions amplified, and the laboratory in partitioned and assigned its own best-fitting model of evolution, which each sample was analyzed, see Table 2. Details of the as determined with MODELTEST 3.06 (16). For both data sets, one methods and precautions for DNA extraction, amplification, and cold chain and three heated chains were run simultaneously for sequencing used at the Allan Wilson Centre are essentially as 2 million generations, and 1 tree per 1,000 was sampled. The first outlined in the supplemental material in refs. 3 and 12. Briefly, 100 trees were discarded as burn-in, and Bayesian posterior DNA was extracted from Ϸ0.2 g of moa bone shavings in 0.5 M probabilities were estimated on the 50% majority rule consensus EDTA with proteinase K. Samples were purified by phenol͞ of the remaining 1,900 trees. Analyses were repeated four times chloroform extraction and then concentrated by using Vivaspin and recovered the same topology. Trees were
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