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The Timing of Diversification Within the Most Divergent Parrot Clade

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The Timing of Diversification Within the Most Divergent Parrot Clade Journal of Avian Biology 45: 140–148, 2014 doi: 10.1111/j.1600-048X.2013.00200.x © 2013 T e Authors. Journal of Avian Biology © 2013 Nordic Society Oikos Subject Editor: Martin Paeckert. Accepted 25 October 2013 The timing of diversifi cation within the most divergent parrot clade Frank E. Rheindt , Les Christidis , Sylvia Kuhn , Siwo de Kloet , Janette A. Norman and Andrew Fidler F. E. Rheindt ([email protected]), Dept of Biological Sciences, National Univ. of Singapore, 14 Science Drive 4, Singapore 129801, Singapore, and: Dept of Organismic and Evolutionary Biology, Harvard Univ., USA. – L. Christidis, National Marine Science Centre, Southern Cross Univ., Australia, and: Dept of Genetics, Univ. of Melbourne, Australia. – S. Kuhn, Max Planck Inst. for Ornithology, Seewiesen, Germany. – S. de Kloet, Animal Genetics Inc., Tallahassee, Florida, USA. – J. A. Norman, Dept of Genetics, Univ. of Melbourne, Australia. – A. Fidler, Inst. of Marine Science, Univ. of Auckland, New Zealand. T e Strigopidae are an ancient parrot (Psittaciformes) family consisting of three extant species placed in two genera ( Nestor, Strigops ) and restricted to New Zealand. T eir evolutionary history is clouded because the timing of divergence events within this family has variously been attributed to Pleistocene climate change or much earlier earth-historic events. Here we examine new psittaciform DNA sequence data, and combine them with previously published sequences, to shed light on the poorly understood timing of diversifi cation within the Strigopidae. Using calibrations indirectly derived from both psittaciform and non-psittaciform fossils, our data indicate a Late Pliocene or Early Pleistocene (ca 1.2 – 3.6 mya) diff erentiation between the two Nestor species (kea and kaka), possibly in response to shifts in habitat distribution associated with sea level fl uctuations. T e unique, monotypic, nocturnal and fl ightless genus Strigops (kakapo) is shown to have diverged from the Nestor lineage probably ca 28 – 29 mya, coinciding with the potential Oligocene submergence of Zealandia when much of its landmass may have been fragmented into smaller islands, providing a setting for allopatric diversifi cation. T e rifting of Gondwana has been implicated as a major divergence time in question is the same as the geologic driver of early parrot (Psittaciformes) and perching bird vicariance event used for calibration (Schweizer et al. 2011). (Passeriformes) diversifi cation, largely based on the geo- Fossils provide an alternative approach for calibrating graphic restriction to New Zealand (NZ) of extant basal the dating of parrot diversifi cation. T e psittaciform clade members from both these orders (Ericson et al. 2002, fossil record mostly consists of Pleistocene and Pliocene Barker et al. 2004, Wright et al. 2008). T e two orders also fi nds that can be identifi ed to the level of extant genera appear to be sister groups (Hackett et al. 2008, Suh et al. (Tonni and Noriega 1996, Boles 1998, Stidham 2009, 2011, McCormack et al. 2013). Within Psittaciformes, the Tambussi et al. 2009). T e only older parrot fossils include earliest divergence is between the NZ-restricted family a Miocene (ca 16 mya) cacatuid fragment which is identi- Strigopidae (kakapo, kea and kaka) and other parrots, fol- fi able to modern genus level (Boles 1993) and Eocene to lowed by divergence between the Australasian cockatoos mid-Miocene members of extinct taxa that have shed (Cacatuidae) and remaining parrots (Psittacidae) (de Kloet much light on early parrot evolution but are often diffi - and de Kloet 2005, Tavares et al. 2006, Wright et al. cult to place on the phylogenetic tree (Wetmore 1926, 2008; for family-level classifi cation see Christidis and Boles Mayr 1998, 2007, Ml í kovsky 1998, Cheneval 2000, Mayr 2008). Accordingly, the split between the Strigopidae and and G ö hlich 2004, Waterhouse et al. 2008), although other parrots has been suggested to have resulted from some of them were conclusively identifi ed as members vicariance associated with the Cretaceous rifting of the of stem-group parrots (Mayr 1998, 2007, Waterhouse microcontinent ‘ Zealandia ’ from Gondwana ca 83 – 85 mya et al. 2008). On account of this sparse parrot fossil record, (McLoughlin 2001, Wright et al. 2008). However, the tim- combinations of both psittaciform and non-psittaciform ing of subsequent diversifi cation events within Strigopidae fossils have been used to provide calibration points for is still poorly known, and its Cretaceous origin has been the estimating the basal split between Strigopidae and other subject of controversy: using the proposed timing of parrots (Pacheco et al. 2011, Schweizer et al. 2011, White the separation of Zealandia from Gondwana to date the et al. 2011). Using six avian fossil-calibrated points in divergence between the Strigopidae and other parrots combination with full mitochondrial genome sequences, has been suggested to be a circular argument because the White et al. (2011) produced estimates of the basal split 140 between Strigopidae and other Psittaciformes at ca 36 – 59 this study are interpreted against a range of possible earth- mya. Pacheco et al. (2011), using three fossil calibration historic events. points and Ͼ 70 avian mitochondrial genomes, obtained a date of 57 – 61 mya for the same split. Importantly, the results of Pacheco et al. (2011) were not changed Material and methods when an 85 mya separation of Zealandia from Gondwana was postulated as a fourth calibration point for the most Genomic DNA preparation, sequencing and basal split within the perching birds included in their sampling strategy analysis. Schweizer et al. (2011), using a dataset compris- ing three nuclear genes in combination with three fossil Following Fidler et al. (2004) (strigopid taxa) or de Kloet points, one of which diff ered from Pacheco et al. (2011), and de Kloet (2005) (all remaining taxa), genomic DNA obtained a date of 45 – 72 mya for the basal split of was isolated from blood or feather samples of individuals Strigopidae and other Psittaciformes. from 14 psittaciform species spanning all three families, T e fossil-based estimates for psittaciform diversifi ca- including the three extant species of the Strigopidae, three tion events reported in these studies (Pacheco et al. Cacatuidae and eight Psittacidae (Table 1). AANAT was 2011, Schweizer et al. 2011, White et al. 2011) are in good amplifi ed from all 14 genomes, while COI was amplifi ed agreement with estimates of the Cacatuidae – Psittacidae from four species (Table 1). We sourced from the literature split obtained from studies examining Neoavian diversifi - sequence data for the following genes (Table 1): [mtDNA] Ͼ cation utilizing 20 independent avian fossil calibrations COI (Russello and Amato 2004, Wright et al. 2008), and a spectrum of sequence data and analytical methods NADH dehydrogenase subunit 2 (ND2) (Eberhard and (Ericson et al. 2006, Brown et al. 2007, 2008). T ese Bermingham 2004, Joseph et al. 2008, Wright et al. 2008); Paleocene to Eocene divergence estimates have been inter- [nuclear DNA] rhodopsin intron 1 (Rho1), transforming preted as supporting strigopid overwater dispersal to NZ growth factor β 2 intron 5 (TGFB), tropomyosin intron long after Zealandia had separated from Gondwana at (Trop), spindlin intron III (SpinIII) (de Kloet and de 83 – 85 mya (Waters and Craw 2006, Goldberg et al. 2008, Kloet 2005, Hackett et al. 2008, Wright et al. 2008). T e Schweizer et al. 2010, 2011). full dataset therefore included two mtDNA and fi ve nuclear A further complication in elucidating the timing of loci, although Nestor meridionalis was only represented by strigopid diversifi cation is that evidence for continuous AANAT, COI and spindlin (Table 1). For seven genera (Ara , land in present-day NZ throughout the Oligocene is Amazona, Aratinga, Psittacula, Cacatua, Lorius, Platycercus), equivocal (Trewick et al. 2006, Waters and Craw 2006, sequences for some of the loci were only available for Goldberg et al. 2008, Landis et al. 2008, Trewick and Gibb closely related congeners of the species for which we gener- 2010). While present-day NZ may have been largely sub- ated AANAT sequences (Table 1). In these cases we utilized merged during the ‘ Oligocene drowning ’ it is possible that such congeneric sequences only when there is no doubt large landmasses were present in currently-submerged about generic allocation. T is was only an issue for some oceanic parts of Zealandia during that time (Meff re et al. non-strigopid lineages that were not the main focus of 2006). While ‘ Oligocene drowning ’ remains controversial, this study. it has been invoked to suggest that the present-day terres- trial fauna and fl ora of NZ may have descended from arrivals dispersing here over the past 23 million yr (Trewick Amplifi cation of AANAT and COI sequences et al. 2006, Waters and Craw 2006, Goldberg et al. 2008, Trewick and Gibb 2010). For AANAT amplifi cation, the following primers were We combine novel and published DNA data to used in combination with the GC-rich PCR system (Roche better elucidate the timing of diversifi cation within the Diagnostics, Germany): 5 ′ -RGCGCGKTGCCKTTCCTGA Strigopidae. Our study reports new sequence data for AGCC-3 ′ (forward); 5 ′ -CGCTGTTCCTGCGCATGAA 14 psittaciform species, including all three members of GGCATG-3 ′ (reverse). We used the following reaction the Strigopidae, from the nuclear arylalkylamine N - conditions: 95 ° C/3 min; 95 ° C/30 s, 58° C/30 s, 72 ° C/90 s, acetyltransferase (AANAT) gene (ca 1.7 – 2.5 kb depending ten cycles; 95 ° C/50 s, 62 ° C/30 s, 72 ° C/90 s increasing on intron length), encompassing three coding exons and 5 s per cycle, 25 cycles; 72 ° C/7 min, 15 ° C/hold. Partial two introns (Supplementary material Appendix 1, Fig. A1). COI sequences were amplifi ed using the primers LCOIp T is gene was previously used successfully in avian phylo- and HCOIp of Wright et al.
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