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The Evolutionary History of Moas

The Evolutionary History of Moas

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Published by draculavanhelsing
The evolutionary history of the extinct ratite moa
and New Zealand Neogene paleogeography
The evolutionary history of the extinct ratite moa
and New Zealand Neogene paleogeography

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Published by: draculavanhelsing on Mar 24, 2012
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The evolutionary history of the extinct ratite moaand New Zealand Neogene paleogeography
M. Bunce
a,1,2
, T. H. Worthy
b,c,1
, M. J. Phillips
d
, R. N. Holdaway
e
, E. Willerslev
f
, J. Haile
f,g
, B. Shapiro
g,h
, R. P. Scofield
i
,A. Drummond
 j
, P. J. J. Kamp
k
, and A. Cooper
b,2
a
Ancient DNA Laboratory, School of Biological Sciences and Biotechnology, Murdoch University, Perth 6150, Australia;
b
Australian Centre for Ancient DNA,University of Adelaide, South Australia 5005, Australia;
c
School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney,New South Wales 2052, Australia;
d
Centre for Macroevolution and Macroecology, Research School of Biology, Australian National University, Canberra2601, Australia;
e
Palaecol Research Ltd and School of Biological Sciences, University of Canterbury, Christchurch 8041, New Zealand;
f
Centre for AncientGenetics, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
g
Department of Zoology, University of Oxford, OxfordOX13PS, United Kingdom;
h
Department of Biology, Pennsylvania State University, University Park, PA 16802;
i
Canterbury Museum, Rolleston Avenue,Christchurch 8013, New Zealand;
j
Bioinformatics Institute and Department of Computer Sciences, University of Auckland, Auckland 1020, New Zealand;and
k
Department of Earth and Ocean Sciences, University of Waikato, Hamilton 3240, New ZealandEdited by James P. Kennett, University of California, Santa Barbara, CA, and approved September 24, 2009 (received for review June 28, 2009)
The ratite moa (Aves: Dinornithiformes) were a speciose group ofmassive graviportal avian herbivores that dominated the New Zea-land (NZ) ecosystem until their extinction
600 years ago. Thephylogeny and evolutionary history of this morphologically diverseorderhasremainedcontroversialsincetheirinitialdescriptionin1839.We synthesize mitochondrial phylogenetic information from 263subfossil moa specimens from across NZ with morphological, ecolog-ical, and new geological data to create the first comprehensivephylogeny, taxonomy, and evolutionary timeframe for all of thespecies of an extinct order. We also present an important newgeological/paleogeographical model of late Cenozoic NZ, which sug-geststhatterrestrialbiotaontheNorthandSouthIslandlandmasseswereisolatedformostofthepast20–30Ma.Thedatarevealthatthepatternsofgeneticdiversitywithinandbetweendifferentmoacladesreflect a complex history following a major marine transgression inthe Oligocene, affected by marine barriers, tectonic activity, andglacialcycles.Surprisingly,theremarkablemorphologicalradiationofmoa appears to have occurred much more recently than previousearly Miocene (
ca.
15 Ma) estimates, and was coincident with theaccelerated uplift of the Southern Alps just
ca.
5–8.5 Ma. Togetherwith recent fossil evidence, these data suggest that the recentevolutionary history of nearly all of the iconic NZ terrestrial biotaoccurred principally on just the South Island.
ancient DNA
Oligocene Drowning
Dinornithiformes
phylogeny
taxonomy
T
he prolonged geographic isolation of New Zealand (80–60million years) and the paucity of terrestrial mammals created aunique ecosystem dominated by an estimated 245 species of birds(1), providing an unparalleled opportunity to observe evolutionaryprocesses. The most striking of the recent avian radiations is that of the extinct ratite moa (Aves: Dinornithiformes), a speciose orderranging in size from a large turkey to the 3 m tall
Dinornis
weighingup to 300 kg. Ratites are a basal lineage of birds that are hypoth-esized to have had a common ancestor
ca.
80 million years ago onthe Cretaceous southern supercontinent of Gondwana, which sub-sequently underwent either vicarious speciation as the landmassfragmented (2), and/or flighted dispersal (3). The extant membersof the ratite lineage include the ostrich (Africa), emu, cassowary(Australia, New Guinea), rhea (South America), and kiwi (NZ).Extinct ratites include the giant elephant birds (Madagascar) andmoa (NZ).Since the first description in 1839 (4) the taxonomy of moa hasremained contentious with up to 64 different species and 20 generaassignedatvarioustimes(1).ThecomplexgeologicalhistoryofNZ,and significant regional variations in climate, diet, and sexualdimorphism (SD) have resulted in moa being highly variablemorphologically, complicating attempts to define species limits.Morphometric and osteological studies have generally recognizedtwo families, Emeidae and Dinornithidae (Table S1), which most recently have been considered to contain eight and three speciesrespectively (1, 5–7). The recovery, amplification, and sequencingof ancient DNA from fossil bone has provided new insights intomoa systematics, and revealed extreme cases of SD (8–14). Fig. 1depicts the current taxonomy of moa (including changes proposedin this article), as well as summarizing species distributions, dimen-sions, and ecology.InthisstudyweusemitochondrialDNAsequencesisolatedfrom119specimens,inadditiontopreviouslypublisheddata(9–13),tostudythemode and tempo of moa evolution, phylogeography, and taxonomy,and relate this to the geological and ecological history of NZ.
Results and Discussion
The accuracy of studies employing molecular clocks to datespeciation events is becoming increasingly scrutinized. Problemsassociated with calibration points, substitution saturation, basecomposition bias, model selection, and more recently with thetimedependencyofmolecularclocks,canalldistortthetemporalaccuracy of phylogenetic reconstructions (15–18). We used twocontrasting approaches in an attempt to establish timeframes forthe divergence events within and between moa species: anexternally (fossil) calibrated analysis of avian mitochondrialprotein-coding sequences, and an internally calibrated Bayesiananalysis of radiocarbon-dated moa mitochondrial control regionsequences.For the externally calibrated approach, two datasets (designatedmtg-10,692 and mtg-2,153) were generated from existing moaGenBank data (9–13, 19) (DatasetS1andDatasetS2). We followed the procedure of Baker et al. (9) anddated the branching events at the base of the moa phylogeny using a 10,692 bp dataset(mtg-10,692) comprising mitochondrial coding region sequencesfrom 26 avian taxa (including 9 ratites), which was externallycalibrated from the fossil record (
SI Te xt
andTable S2). We used a variety of methods to deal with biases introduced b y substitution saturation and phylogenetic artifacts(
SI Te xt
), and estimateddivergencedatesusingBEASTv.1.4.8(20)asdescribedin
 Methods
.
Authorcontributions:A.C.designedresearch;M.B.,E.W.,J.H.,P.J.J.K.,andA.C.performedresearch;M.B.,T.H.W.,M.J.P.,R.N.H.,B.S.,R.P.S.,A.D.,P.J.J.K.,andA.C.analyzeddata;andM.B., T.H.W., M.J.P., and A.C. wrote the paper.The authors declare no conflict of interest.This article is a PNAS Direct Submission.Datadeposition:ThesequencesreportedinthispaperhavebeendepositedintheGenBankdatabase (accession nos. GU138993–GU139113).
1
M.B. and T.H.W. contributed equally to this work.
2
To whom correspondence may be addressed. E-mail: alan.cooper@adelaide.edu.au orm.bunce@murdoch.edu.au.This article contains supporting information online atwww.pnas.org/cgi/content/full/ 0906660106/DCSupplemental.
www.pnas.org
cgi
doi
10.1073
pnas.0906660106 PNAS Early Edition
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The resulting posterior distribution of the molecular date estimatefor the basal moa branch was then used to calibrate analyses withina shorter dataset of 2153 bp (9) of 29 moa mitochondrial proteincodingsequences(mtg-2,153,TableS2)toobtaindateestimatesfor species-level divergences within themoa phylogeny.For the internally calibrated approach, an alignment of 80
 Megalapteryx
,
Dinornis
, and
Pachyornis
control region sequences(389 bp) from radiocarbon-dated moa bones (TableS3) were used as calibration points (or ‘‘time-stamped’’ data) to temporally cali-brate a Bayesian framework using BEAST (21).
Moa Systematics at Family and Genus Level.
Bayesian analysis ofthemtg-2,153 mitochondrial coding region dataset (2,153 bp for 29moa)yieldedthemaximum
 aposteriori
(MAP)treeshowninFig.2. Similar analysis of the control region data from 263 moacontrol region sequences (389 bp) yielded the higher resolutiontree shown in Fig. 3 (presented in detailinFig.S1), and more detailed analyses with restricted taxonomic coverage shown inFig. 4. The phylogenetic arrangement in Figs. 2 and 3 has anumber of discrepancies with current taxonomic arrangements(TableS1) in which just two families (Dinornithidae and Emei- dae) are recognized, with two subfamilies within Emeidae(Megalapteryginae and Anomalopteryginae). Although thesethree main lineages are recovered in analyses of the mtg-2153mitochondrial coding region dataset (Fig. 3),
Megalapteryx
isclearly the basal moa lineage. This arrangement is consistent with previous genetic studies (9, 11, 12), and recent analyses of morphological characters (1, 22), where
Megalapteryx didinus
falls as the basal moa lineage, and is outside Emeidae. Conse-quently, we propose that moa taxonomy be revised so that threefamilies are recognized in the Dinornithiformes (Table S1): Dinornithidae (
 Dinornis
); Emeidae (
 Pachyornis
,
 E meus
,
 Ano ma- lopteryx
,
Euryapteryx
), and Megalapterygidae (new family; typeand only genus
Megalapteryx
). Neither of the presently recog-nized subfamilies (Anomalopteryginae, Emeinae) is supportedby either morphological cladistics (1, 22) or mtDNA analyses (9,13), and should be discarded. At the genus level, there is strongsupport (posterior probabilities of 100%) (Fig. 3) for all six moagenera outlined by Cracraft (7) and refined by Worthy andHoldaway (1).Thesuggestionthatspeciescanberecognizedsolelyfromgeneticdistances has previously been identified as problematic (23, 24).Suggestionsthatthisapproachcanalsobeappliedtothesystematicstudiesofcloselyrelatedextincttaxa(9)areparticularlyconcerninggiven the lack of behavioral and ecological data. This problem isexemplified by the strong phylogeographic pattern exhibited withinthe alpine moa
M. didinus
(Fig. 4 andFig.S1) where control region genetic distances of 4.7% separatemtDNA‘‘clades’’. This distanceis greater than that between well recognized genera such as
Emeus
and
Euryapteryx
(4.5%), and reinforces the idea that such geneticdiversity measures are a product of population longevity and nichepersistence, as well as other population parameters. Keeping thisobservation in mind, and integrating recent morphological studiesand moa palaeoecological and phylogeographical data, we reviewthe taxonomic status of all moa genera (
SI Te xt
) and propose the
Fig.1.
Systematics,dimensions,andapproximatedistributionsofmoainthethree family, six genera, nine species taxonomy advocated in this study.Estimates of body size and habitat were generated from information con-tainedinWorthyandHoldaway(2002)andarediscussedinmoredetailinthe
SI Text 
. A comparison with the generally accepted two family, 11 speciesclassification used from the 1980’s to 2002 is presented inTable S1.
Fig. 2.
A spatial and temporal context for the evolution of moa. Molecularphylogeny and date estimates of the moa radiation generated from themtg-2,153 dataset (see
Methods
), compared with the new paleogeographicmodel of Neogene New Zealand. A Bayesian Inference tree is shown withBayesian posterior probability values (
80%) indicated on the nodes withsupport, whereas the node bars correspond to the 95% HPD. A series of fourpaleogeographic maps, based on extensive geological mapping of the area(see
Methods
and
SI Text 
), show different time horizons during the Neogeneand the presence/absence of North and South Island landmasses in centralNew Zealand. The uplift of the Southern Alps (
ca.
5–8.5 million years) andperiodic bridging to the North Island in the Pleistocene (
2 million years)appear to be instrumental in moa speciation. The absence of deep (
ca.
20Million years) splits in the moa phylogeny suggest that all recent moa speciesoriginated from the southern landmass (see main text), consistent with thephylogeographic distributions (Fig. 3, Fig. 4
B
, and
SI Text 
).
2 of 6
www.pnas.org
cgi
doi
10.1073
pnas.0906660106 Bunce et al.
 
new taxonomic arrangement shown in Fig. 1 andTableS1. Overall,  we have adopted a conservative approach tospecies designationsand regard mtDNA diversity alone as insufficient to define specieslimits, especially in the context of recognized barriers to gene flow(discussed later in
Island Allopatry and Pleistocene Cycles
). As newDNA profiling approaches are devised (25) there may be minorfuturealterationstothetaxonomicframework(3families,6genera)proposed here.
Establishing a Timeframe for Moa Evolution.
Reanalysis of existing mtDNA data.
The mean divergence date between Dinornithidaeand Emeidae was estimated at just 5.27 Ma [95% highestprobability density (HPD): 3.1–9.0] in the BEAST analysis of themtg-10,692 dataset, with 3rd codon positions RY-coded, andusing two ratite and three nonratite calibration priors (
SI Te xt
andTable1).Thisdateislessthanhalftheageofthe15Ma(95%CI 14.5–15.6 Ma) date inferred using penalized likelihood in r8sused by Baker et al. (9), which we also recovered in r8s analysesof the mtg-10,692 dataset using standard nucleotide coding (15.8Ma). Importantly although, this estimate drops to 8.1 Ma whenRY-coding is used to reduce the impact of saturated 3rd codonpositions (
SI Te xt
). The estimate drops further, to 7.6 Ma, if theproblematic calibration date of 82 Ma for the beginning of rafting between New Zealand and Australia/Antarctica is dis-carded in favor of other, more secure, avian calibrations (
SI Te xt
). Because this geological event would not preventthedispersal of flying paleognaths, it is now questionable (3).It appears that the differences between our analysis and that of Bakeretal.(9)arenotprimarilywiththeprogramsused,butrathertheuseofthesaturated3rdcodonpositionsandtheproblematic82Ma calibration. When these issues are dealt with, r8s infers a dateof 7.6 Ma, well within the 95% HPD of the BEAST analysis.Overall, we prefer the BEAST estimate to those of r8s because thelatter assumes autocorrelated rate changes among branches, whichisnotsupportedbycovarianceanalysiswithinourBEASTanalyses.Consequently, we calibrated the larger moa mtg-2,153 bp dataset with the lognormal approximation of the posterior distribution forthe Dinornithidae/Emeidae split from the mtg-10,692 analysis, andused this to estimate a variety of divergence dates within moaevolution (Table 1). In line with the above results, the datingestimates described in Table 1 are considerably more recent thanpreviouslysuggested(11,19).Interestingly,thenew5.8Maestimatefor the basal divergence of 
Megalapteryx
correlates closely with therapid phase of mountain uplift during the Miocene-Pliocene. It isalso notable that there is no moa fossil evidence (26) that contra-dicts the timeframe proposed here.
Internally calibrated time-stamped data.
BEAST analysis of the radio-carbon-dated
 Megalapteryx
,
 Dinornis
,and
 Pachyornis
controlregionsequences (see
Methods
and
SI Te xt
) provided an estimated mu-tation rate of 8.7% per million years (95% HPD 2.34–20.4%). The
South island fossilsNorth island fossils
Family: DinornithidaeFamily: MegalapteryidaeFamily: Emeidae
100100100100100848510010010098991001001009910098100
DinornisrobustusDinornisnovaezealandiaeMegalapteryx didinusPachyornisaustralisPachyorniselephantopusPachyornisgeranoides Anomalopteryx didiformisEmeuscrassusEuryapteryx curtus
Root of moatree10010010099871000.05
Fig. 3.
Phylogenetic reconstruction of all moa species. The maximum
a posteriori 
(MAP) tree of 263 mitochondrial control region sequences of eachofthemoageneraasgeneratedinBEAST(
Methods
)usingaHKY
G
Imodelon a 389 bp alignment. A more detailed tree in which the tips are visible ispresented inFig. S1. DNA sequences obtained from North and South Islandfossils arecoloredred and blue respectively, and suggest that North Islandspecimenstendtooccupyderivedphylogeneticpositions(seealsoFig.4
B
and
SI Text 
). For clarity, posterior probabilities are shown only on basal nodes.Saturation effects in the control region data have resulted in the root of themoa tree being misplaced in this MAP tree, and the mitochondrial proteincoding data (Fig. 2) is predicted to give a better estimate of the branchingtopology at the base of the moa radiation.
   C   l  a   d  e
    A   C   l  a   d  e   B   C   l  a   d  e   C    C   l  a   d  e   D 
10010091100100100851007499
 
91
DC AB
     E    m    e    u    s     E    u    r    y    a    p     t    e    r    y    x
North island fossils
1001001007154969965
South island fossils
AB
Fig. 4.
Phylogenetic reconstruction of
Megalapteryx 
(
 A
) and
Emeus
 / 
Euryapteryx 
(
B
) using mtDNA control region data. Localities of the moafossils are indicated on the tip labels together with ages of fossils (AMS
14
Cdates and error) where known. The original morphological identificationsare given as a 4 letter abbreviation, with sample, museum, and GenBanknumberswhererelevant.ThetreesshownhereareMAPtreesgeneratedinBEAST (
Methods
) using
Dinornis
or
Pachyornis
, respectively, as outgroups.Posterior probabilities are shown on nodes with support. Deep phyloge-netic splits in
Megalapteryx 
(
 A
) are caused by prolonged periods of geo-logicalisolationresultinginfourdistinctSouthIslandclades(A-D).Thelackof diversity in
Emeus
and lack of North-South monophyly in
Euryapteryx 
demonstrates a complex evolutionary history involving bottlenecks andperiodicgeneflowbetweentheNorthandSouthIslandsinthePleistocene.The phylogenetic position of North Island
Euryapteryx 
specimens supportsa southern origin for this species.
Bunce et al. PNAS Early Edition
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