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Diversification of Petroica Robins Across the Australo-Pacific Region: First Insights Into the Phylogenetic Affinities of New Guinea’S Highland Robin Species

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Diversification of Petroica Robins Across the Australo-Pacific Region: First Insights Into the Phylogenetic Affinities of New Guinea’S Highland Robin Species Emu - Austral Ornithology ISSN: 0158-4197 (Print) 1448-5540 (Online) Journal homepage: http://www.tandfonline.com/loi/temu20 Diversification of Petroica robins across the Australo-Pacific region: first insights into the phylogenetic affinities of New Guinea’s highland robin species Anna M. Kearns, Leo Joseph, Aude Thierry, John F. Malloy, Maria Nandadevi Cortes-Rodriguez & Kevin E. Omland To cite this article: Anna M. Kearns, Leo Joseph, Aude Thierry, John F. Malloy, Maria Nandadevi Cortes-Rodriguez & Kevin E. Omland (2018): Diversification of Petroica robins across the Australo- Pacific region: first insights into the phylogenetic affinities of New Guinea’s highland robin species, Emu - Austral Ornithology, DOI: 10.1080/01584197.2018.1498744 To link to this article: https://doi.org/10.1080/01584197.2018.1498744 View supplementary material Published online: 06 Aug 2018. Submit your article to this journal View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=temu20 EMU - AUSTRAL ORNITHOLOGY https://doi.org/10.1080/01584197.2018.1498744 Diversification of Petroica robins across the Australo-Pacific region: first insights into the phylogenetic affinities of New Guinea’s highland robin species Anna M. Kearns a,b, Leo Josephc, Aude Thierryd, John F. Malloya, Maria Nandadevi Cortes-Rodrigueza,e and Kevin E. Omlanda aDepartment of Biological Sciences, University of Maryland, Baltimore, USA; bCenter for Conservation Genomics, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, USA; cAustralian National Wildlife Collection, CSIRO National Research Collections Australia, Canberra, Australia; dSchool of Biological Sciences, University of Canterbury, Christchurch, New Zealand; eDepartment of Biology, Center for Natural Sciences, Ithaca College, Ithaca, USA ABSTRACT ARTICLE HISTORY Complex spatial and temporal phylogenetic patterns have emerged among Pacific Island radiations Received 13 December 2017 and their Australian and New Guinean congeners. We explore the diversification of Australo-Pacific Accepted 1 July 2018 Petroica robins using the first phylogeny with complete species-level sampling of the genus. In doing KEYWORDS so we provide the first assessment of the phylogenetic affinities of two poorly known species with Australian birds; highly restricted ranges in the highlands of New Guinea – Subalpine Robin (Petroica bivittata)and biogeography; conservation; Snow Mountain Robin (P. archboldi). Our analyses suggest that Petroica underwent an initial diversi- evolution; genetics; Pacific fication during the Plio-Pleistocene that established four major lineages restricted to New Zealand Ocean; threatened species; (four species), Australia (four species), New Guinea (two species) and Pacific Islands + Australia (three taxonomy or four species). All lineages appear to have undergone species diversification in situ with the exception of the Pacific Islands + Australia lineage where long-distance over-water dispersal must be invoked to explain the placement of the Red-capped Robin (P. goodenovii) within the iconic Pacific robin species complex (P. multicolor + pusilla). Two scenarios fit this biogeographic pattern: (1) a single ‘upstream’ colonisation of mainland Australia from a Pacific Island ancestor resulting in P. goodenovii,or(2)twoorthree‘downstream’ colonisations from a mainland Australian or New Guinean ancestor resulting in the distinct Pacific robin lineages that occur in the south-west Pacific. Overall, biogeographic patterns in Petroica suggest that long-distance dispersal and island colonisa- tions have been rare events in this group, which contrasts with other Australo-Pacific radiations that show evidence for repeated long-distance dispersals and multiple instances of secondary sympatry on islands across the Pacific. Introduction temporally complex phylogenetic signatures within the Australo-Pacific biota that pose considerable chal- Patterns of biodiversity in the Australo-Pacific region lenges for developing robust hypotheses (Ericson et al. (Australia, New Guinea, New Zealand and south-west 2002; Filardi and Moyle 2005; Jønsson et al. 2010, 2011; Pacific Islands) have originated through a diverse range Cibois et al. 2011, 2014; Joseph et al. 2011; Irestedt of colonisation and diversification scenarios. Both the et al. 2013; Andersen et al. 2014a,2015; Schweizer et al. timing and routes of colonisation have varied – many 2015). For example, the extent to which the Australo- involving ‘downstream’ dispersal of colonists from Pacific biota have experienced concordant vs. taxon- mainland Australia to the Pacific Islands, others from specific idiosyncratic diversification histories remains ‘upstream’ dispersal from the Pacific Islands to unclear owing to the difficulty in teasing apart signa- Australia (MacArthur and Wilson 1967; Filardi and tures left by older vs. more recent processes (e.g. intra- Moyle 2005; Bellemain and Ricklefs 2008; Jønsson archipelago colonisations leading to secondary sympa- et al. 2010; Cibois et al. 2011; Schweizer et al. 2015). try). Another continuing issue for studies of this region Pacific Island radiations have also been shaped by is the limited availability of scientific collections for key repeated exchange of colonists among islands resulting taxon groups such as widespread Pacific Island radia- in secondary sympatry of divergent non-sister lineages tions, with numerous distinct island forms scattered (Andersen et al. 2015). These diverse colonisation and across Melanesia, Oceania and Polynesia (i.e. the diversification histories have left geographically and CONTACT Anna M. Kearns [email protected] Supplemental data for this article can be accessed here. © 2018 BirdLife Australia 2 A. M. KEARNS ET AL. ‘great speciators’) (Diamond et al. 1976; Mayr and 2016). Critically, the lack of complete taxonomic sam- Diamond 2001), and species with restricted ranges in pling in previous phylogenetic studies has hindered remote areas of New Guinea. One of the main gaps in robust tests of these hypotheses. No previous study had our knowledge stemming from these issues is under- complete species sampling of all members of the above standing the extent to which New Guinea has acted as three major lineages, and none have sampled the two an important island ‘stepping-stone’ enabling colonisa- species that are restricted to the highlands of New tion between Australia and the south-west Pacific (see Guinea – the Subalpine Robin Petroica bivittata (De Filardi and Moyle 2005). Vis, 1897) and the Snow Mountain Robin Petroica arch- Recent work on the Australo-Pacific robins (Aves: boldi (Rand 1940) (see Figure 1 for species ranges). Petroicidae: Petroica) illustrates the limitations of having Here,weprovidethefirstanalysisofthephylogenetic incomplete taxonomic and geographic sampling for placement of New Guinea’s P. archboldi and P. bivittata, developing robust biogeographic hypotheses (Miller and and in doing so present the first phylogeny for Petroica with Lambert 2006; Loynes et al. 2009;Christidiset al. 2011; complete species sampling. Like many of New Guinea’s Kearns et al. 2016). Petroica robins are a charismatic highland species, little is known of the behaviour, life group of passerines known for their striking variability history, precise range limits and taxonomic affinities of P. in plumage carotenoids, repeated losses and gains of archboldi and P. bivittata. Plumage and body size strongly sexual dichromatism among island and mainland forms differentiate the two species (Boles 2007;seeFigure 1 for and diversification of species across the Australo-Pacific plumage differences), and they also show differences in region (Boles 2007). The 13 Petroica species are distrib- foraging behaviour and habitat preferences – P. archboldi uted across a range of habitats in Australia, New Zealand, is the only bird inhabiting the highest rocky scree habitats New Guinea and the south-west Pacific (Bougainville, at 3800–4200 m elevation (Pratt and Beehler 2015), while P. Solomon Islands, Vanuatu, Fiji, Samoa, Norfolk Island). bivittata occupies high mountain forest and alpine/subal- Consensus from previous phylogenetic studies supports pine shrublands above 2700–3500 m elevation (Beehler three major lineages within Petroica: (1) New Zealand and Pratt 2016; Figure 1). Given that phylogenetic patterns (four species: P. australis, P. longipes, P. traversi, P. macro- across the rest of Petroica support geography, rather than cephala), (2) Australia (four species: P. rosea, P. rodino- phenotype, as the best predictor of phylogenetic affinities gaster, P. phoenicea, P. boodang) and (3) the Pacific (Kearns et al. 2016), we predict that P. archboldi and P. Islands/Australia (three species: P. multicolor, P. pusilla, bivittata couldbesisterspeciesdespitetheirmajorpheno- P. goodenovii)(MillerandLambert2006; Loynes et al. typic differences. In the absence of recent tissue collections, 2009;Christidiset al. 2011; Kearns et al. 2016). Notably, we use an ancient DNA approach to sequence an informa- the most widespread species in Australia, the Red-capped tive region of mtDNA from museum specimens of P. Robin (P. goodenovii), is more closely related to the archboldi and P. bivittata that were collected by the species in the Pacific Islands than to the other four species American Museum of Natural History between 1898 and in Australia. This biogeographic pattern could result from 1938. Given how little
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