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

Abstract

The ratite moa (Aves: Dinornithiformes) were a speciose group of massive graviportal avian herbivores that dominated the New Zealand (NZ) ecosystem until their extinction approximately 600 years ago. The phylogeny and evolutionary history of this morphologically diverse order has remained controversial since their initial description in 1839. We synthesize mitochondrial phylogenetic information from 263 subfossil moa specimens from across NZ with morphological, ecological, and new geological data to create the first comprehensive phylogeny, taxonomy, and evolutionary timeframe for all of the species of an extinct order. We also present an important new geological/paleogeographical model of late Cenozoic NZ, which suggests that terrestrial biota on the North and South Island landmasses were isolated for most of the past 20-30 Ma. The data reveal that the patterns of genetic diversity within and between different moa clades reflect a complex history following a major marine transgression in the Oligocene, affected by marine barriers, tectonic activity, and glacial cycles. Surprisingly, the remarkable morphological radiation of moa appears to have occurred much more recently than previous early Miocene (ca. 15 Ma) estimates, and was coincident with the accelerated uplift of the Southern Alps just ca. 5-8.5 Ma. Together with recent fossil evidence, these data suggest that the recent evolutionary history of nearly all of the iconic NZ terrestrial biota occurred principally on just the South Island.

Fig. 1.

Systematics, dimensions, and approximate distributions of moa in the three family, six genera, nine species taxonomy advocated in this study. Estimates of body size and habitat were generated from information contained in Worthy and Holdaway (2002) and are discussed in more detail in the SI Text. A comparison with the generally accepted two family, 11 species classification used from the 1980's to 2002 is presented in Table S1.

Fig. 2.

A spatial and temporal context for the evolution of moa. Molecular phylogeny and date estimates of the moa radiation generated from the mtg-2,153 dataset (see Methods), compared with the new paleogeographic model of Neogene New Zealand. A Bayesian Inference tree is shown with Bayesian posterior probability values (>80%) indicated on the nodes with support, whereas the node bars correspond to the 95% HPD. A series of four paleogeographic maps, based on extensive geological mapping of the area (see Methods and SI Text), show different time horizons during the Neogene and the presence/absence of North and South Island landmasses in central New Zealand. The uplift of the Southern Alps (ca. 5–8.5 million years) and periodic bridging to the North Island in the Pleistocene (<2 million years) appear to be instrumental in moa speciation. The absence of deep (ca. 20 Million years) splits in the moa phylogeny suggest that all recent moa species originated from the southern landmass (see main text), consistent with the phylogeographic distributions (Fig. 3, Fig. 4B, and SI Text).

Fig. 3.

Phylogenetic reconstruction of all moa species. The maximum a posteriori (MAP) tree of 263 mitochondrial control region sequences of each of the moa genera as generated in BEAST (Methods) using a HKY+G+I model on a 389 bp alignment. A more detailed tree in which the tips are visible is presented in Fig. S1. DNA sequences obtained from North and South Island fossils are colored red and blue respectively, and suggest that North Island specimens tend to occupy derived phylogenetic positions (see also Fig. 4B 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 the moa tree being misplaced in this MAP tree, and the mitochondrial protein coding data (Fig. 2) is predicted to give a better estimate of the branching topology at the base of the moa radiation.

Fig. 4.

Phylogenetic reconstruction of Megalapteryx (A) and Emeus/Euryapteryx (B) using mtDNA control region data. Localities of the moa fossils are indicated on the tip labels together with ages of fossils (AMS ¹⁴C dates and error) where known. The original morphological identifications are given as a 4 letter abbreviation, with sample, museum, and GenBank numbers where relevant. The trees shown here are MAP trees generated in BEAST (Methods) using Dinornis or Pachyornis, respectively, as outgroups. Posterior probabilities are shown on nodes with support. Deep phylogenetic splits in Megalapteryx (A) are caused by prolonged periods of geological isolation resulting in four distinct South Island clades (A-D). The lack of diversity in Emeus and lack of North-South monophyly in Euryapteryx demonstrates a complex evolutionary history involving bottlenecks and periodic gene flow between the North and South Islands in the Pleistocene. The phylogenetic position of North Island Euryapteryx specimens supports a southern origin for this species.