Knapp, Michael; Thomas, Jessica E.; Haile, James; Prost, Stefan; Ho, Simon Y
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Mitogenomic evidence of close relationships between New Zealand's extinct giant raptors and small-sized Australian sister-taxa Knapp, Michael; Thomas, Jessica E.; Haile, James; Prost, Stefan; Ho, Simon Y. W.; Dussex, Nicolas; Cameron-Christie, Sophia; Kardailsky, Olga; Barnett, Ross; Bunce, Michael; Gilbert, M. Thomas P.; Scofield, R. Paul Published in: Molecular Phylogenetics and Evolution DOI: 10.1016/j.ympev.2019.01.026 Publication date: 2019 Document version Publisher's PDF, also known as Version of record Document license: Unspecified Citation for published version (APA): Knapp, M., Thomas, J. E., Haile, J., Prost, S., Ho, S. Y. W., Dussex, N., Cameron-Christie, S., Kardailsky, O., Barnett, R., Bunce, M., Gilbert, M. T. P., & Scofield, R. P. (2019). Mitogenomic evidence of close relationships between New Zealand's extinct giant raptors and small-sized Australian sister-taxa. Molecular Phylogenetics and Evolution, 134, 122-128. https://doi.org/10.1016/j.ympev.2019.01.026 Download date: 25. sep.. 2021 Molecular Phylogenetics and Evolution 134 (2019) 122–128 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Mitogenomic evidence of close relationships between New Zealand’s extinct giant raptors and small-sized Australian sister-taxa T ⁎ Michael Knappa, , Jessica E. Thomasb,c,1, James Hailec,1, Stefan Prostd,e, Simon Y.W. Hof, Nicolas Dussexa,g, Sophia Cameron-Christiea, Olga Kardailskya, Ross Barnettc, Michael Bunceh, M. Thomas P. Gilbertc,i, R. Paul Scofieldj a Department of Anatomy, University of Otago, 270 Great King Street, Dunedin 9016, New Zealand b Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Bangor University, Bangor, UK c Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark d Research Institute of Wildlife Ecology, Vetmeduni Vienna, Vienna, Austria e Department of Integrative Biology, University of California Berkeley, Berkeley, USA f School of Life and Environmental Sciences, University of Sydney, Sydney, Australia g Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden h Trace and Environmental DNA Laboratory, School of Molecular and Life Sciences, Curtin University, Bentley, WA 6102, Australia i Norwegian University of Science and Technology, University Museum, 7491 Trondheim, Norway j Canterbury Museum, 8013 Christchurch, New Zealand ARTICLE INFO ABSTRACT Keywords: Prior to human arrival in the 13th century, two large birds of prey were the top predators in New Zealand. In the Ancient DNA absence of non-volant mammals, the extinct Haast's eagle (Hieraaetus moorei), the largest eagle in the world, and Climate change the extinct Eyles' harrier (Circus teauteensis) the largest harrier in the world, had filled ecological niches that are Extinction on other landmasses occupied by animals such as large cats or canines. The evolutionary and biogeographic Island gigantism history of these island giants has long been a mystery. Here we reconstruct the origin and evolution of New New Zealand megafauna Zealand’s giant raptors using complete mitochondrial genome data. We show that both Eyles’ harrier and Haast’s Trans-Tasman dispersal eagle diverged from much smaller, open land adapted Australasian relatives in the late Pliocene to early Pleistocene. These events coincided with the development of open habitat in the previously densely forested islands of New Zealand. Our study provides evidence of rapid evolution of island gigantism in New Zealand’s extinct birds of prey. Early Pleistocene climate and environmental changes were likely to have triggered the establishment of Australian raptors into New Zealand. Our results shed light on the evolution of two of the most impressive cases of island gigantism in the world. 1. Introduction 15 kg, significantly more heavy than the largest extant eagle, the harpy (Harpia harpyja) at about 9 kg (Worthy and Holdaway, 2002). Haast’s New Zealand’s geographic isolation and lack of non-volant mam- eagle remains have so far only been found in the South Island of New mals has led to a unique avifauna but one that suffered an extinction Zealand. As an adaptation to the mostly forested New Zealand en- rate of ∼50% following human arrival (Worthy and Holdaway, 2002). vironment prior to human arrival, its wings were likely broad but with a Among the most remarkable examples are New Zealand's avian apex limited wingspan of about 2.5–3m (Worthy and Holdaway, 2002). predators, Haast's eagle (Hieraaetus moorei; formerly Harpagornis Haast’s eagle likely preyed on various large moa species, and adaptation moorei) and Eyles' harrier (Circus teauteensis previously referred to as C. to this previously unoccupied niche is thought to have driven the eylesi). Both species have long been recognized as examples of island evolution of the giant body size. gigantism and filled ecological niches that are on other landmasses Eyles’ harrier was a much lighter bird than Haast’s eagle, but with a occupied by animals such as large cats or canines. Haast’s eagle was the weight of ∼3–3.5 kg it was still the largest known harrier in the world. largest known eagle in the world and is estimated to have weighed up to Its wingspan probably reached 2 m. Unlike Haast’s eagle, Eyles’ harrier ⁎ Corresponding author. E-mail address: [email protected] (M. Knapp). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.ympev.2019.01.026 Received 3 October 2018; Received in revised form 22 January 2019; Accepted 31 January 2019 Available online 10 February 2019 1055-7903/ © 2019 Elsevier Inc. All rights reserved. M. Knapp, et al. Molecular Phylogenetics and Evolution 134 (2019) 122–128 was also found in the North Island of New Zealand, but evidence of its samples (spotted harrier). Blood samples were collected from captive presence is so far lacking from the far south of the South Island. It likely individuals during routine veterinary examinations and subsamples of preyed on New Zealand pigeon, kaka, kea and smaller moa species these blood samples were used for DNA analyses. The booted eagle (Worthy and Holdaway, 2002). sample came from a bird at the International Centre for Birds of Prey in The two New Zealand island giants were driven to extinction within Newent, United Kingdom. The little eagle sample came from blood the last 700 years, and most workers consider this to be a result of donated from Perth Raptor Care. The spotted harrier DNA was ex- anthropogenic habitat alteration or competition for resources with the tracted from a liver tissue sample provided by the Australian National growing human population (Bunce et al., 2005; Worthy and Holdaway, Wildlife Collection (CSIRO, Canberra, Australia) to Canterbury Museum 2002). (registration number B53083). DNA was extracted from blood and The evolutionary relationships of Haast’s Eagle were resolved by tissue samples using the Qiagen blood and tissue kit, following the analyses of the mitochondrial cytochrome b gene (Bunce et al., 2005). manufacturer’s instructions. DNA was extracted from 10 μL of blood Surprisingly, Haast’s eagles were found to belonged to a group of small from the samples of little eagle and the booted eagle and from 25 mg of eagles, including the Australasian little eagle (Hieraaetus morphnoides), liver tissue from the spotted harrier. the smallest eagle in the world, and the also small-bodied Eurasian booted eagle (Hieraaetus pennatus). Little eagle weighs less than 1 kg 2.2. DNA sequencing and has a wingspan of 1.1–1.3 m. Booted eagle is only marginally larger. Divergence time estimates suggested that the three lineages di- Prior to sequencing complete mitogenomes, we carried out a pre- verged less than 2 million years ago (Ma), but estimates were based on liminary analysis to identify the Eyles’ harrier’s position and its closest a general avian substitution rate, which is known to be highly variable relative in the global harrier phylogeny (Oatley et al., 2015). For this between lineages (Nabholz et al., 2016). purpose, we amplified a 1027 bp mitochondrial region containing the No genetic analyses of the New Zealand Eyles’ harrier phylogeny genes encoding tRNA-Leu, NADH dehydrogenase subunit 1 (ND1), exists. Based on morphological evidence and biogeographic data, tRNA-Ile, and tRNA-Gln in six overlapping amplicons (see supplemen- Worthy & Holdaway (2002) hypothesised that the taxon was a gigantic tary table S1). Each fragment was amplified twice and sequenced in relative of the extant swamp harrier (Circus approximans), an Aus- both directions on an ABI3730 platform. The consensus was called from tralasian native bird. The swamp harrier has arrived in New Zealand all unambiguous sites (i.e. sites for which sequence data from both naturally at some point in the previous 700 years, potentially filling the amplicons were identical). niche of the then extinct Eyles’ Harrier. The five complete mitogenomes presented in this study were se- Here we analyse the mitochondrial genomes of Haast’s eagle, Eyles’s quenced as part of multiple projects with different objectives. Hence, harrier, and their closest relatives to infer a fossil-calibrated phyloge- different approaches were used to obtain the sequence data. For the netic tree. This allows us to reconstruct the evolutionary histories of the little eagle and booted eagle, DNA from blood extracts was prepared for two New Zealand island giants, along with the environmental and high throughput sequencing by the sequencing service of New Zealand biogeographical changes that are likely to have shaped their evolution. Genomics Limited (NZGL) using a TruSeq library preparation kit and following the manufacturer’s instructions. Sequencing libraries were 2. Materials and methods prepared directly from the DNA extracts and libraries were not enriched prior to sequencing. For the spotted harrier, we amplified the complete 2.1. Samples and DNA extraction mitogenome in two long range amplifications using KAPA Long range PCR enzyme with an annealing temperature of 50C and following the A subfossil femur from Eyles’s Harrier was excavated from Finsch’s manufacturer’s recommendations for a thermal profile.