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A Sympatric Pair of Undescribed White-Eye Species (Aves: Zosteropidae: Zosterops) with Different Origins

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A Sympatric Pair of Undescribed White-Eye Species (Aves: Zosteropidae: Zosterops) with Different Origins applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Zoological Journal of the Linnean Society, 2019, XX, 1–24. With 9 figures. Downloaded from https://academic.oup.com/zoolinnean/advance-article-abstract/doi/10.1093/zoolinnean/zlz022/5477306 by University College Dublin, [email protected] on 24 April 2019 A sympatric pair of undescribed white-eye species (Aves: Zosteropidae: Zosterops) with different origins DARREN P. O’CONNELL1,2*, , DAVID J. KELLY1, NAOMI LAWLESS1, KATIE O’BRIEN1, FIONN Ó MARCAIGH1, ADI KARYA3, KANGKUSO ANALUDDIN3 and NICOLA M. MARPLES1 1 Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin DO2 CX56, Ireland 2 School of Biology & Environment Science, University College Dublin, Dublin DO4 N2E5, Ireland 3 Department of Biology and Biotechnology, Universitas Halu Oleo, Kendari, South-east Sulawesi, Indonesia Received 13 September 2018; revised 15 February 2019; accepted for publication 17 February 2019 Research in the Indo-Pacific region has contributed massively to the understanding of speciation. White-eyes (Aves: Zosteropidae: Zosterops), a lineage containing both widespread ‘supertramp’ species and a high proportion of island endemics, have provided invaluable models. Molecular tools have increased speciation research, but delimiting species remains problematic. We investigated the evolutionary history of Zosterops species in south-east Sulawesi using mitochondrial DNA, morphometric, song and plumage analyses, to draw species limits and assess which techniques offer best resolution. Our investigation revealed a novel Zosterops species, >3000 km from its closest relative. Additionally, we demonstrated unanticipated diversity in the alleged ‘supertramp’ Zosterops chloris and propose the Wakatobi Islands subspecies (Z. c. flavissimus) to be given full species status. Furthermore, we provide the first molecular and phenotypic assessment of the Sulawesi endemic Zosterops consobrinorum. While local populations of this species vary in either genetics or morphometrics, none show consistency across measures. Therefore, we propose no change to Zosterops consobrinorum taxonomy. This study gives insight into one of the great Indo-Pacific radiations and demonstrates the value of using multiple lines of evidence for taxonomic review. KEYWORDS: birds – evolution – Indonesia – islands – new species – Wallacea. INTRODUCTION species (Lohman et al., 2010; Irestedt et al., 2013) and elucidating the evolutionary history of island Islands have long been key to our understanding of colonizations (Cibois et al., 2011, 2014, Andersen et al., evolution, providing discrete geographical units to 2013, 2014). However, questions still remain on how study patterns of speciation and the processes that best to delimit species in widespread radiations (Tobias underlie these patterns (Darwin, 1859; Wallace, 1869). et al., 2010; Andersen et al., 2014), and which processes The islands of the Indo-Pacific have been particularly allow some populations to maintain connectivity over important in the last half-century for laying down large distances, while others become isolated endemic many of the fundamental principles underpinning our taxa (Andersen et al., 2015; Pedersen et al., 2018). understanding of island biogeography and speciation One of the lineages of major importance to the study of (MacArthur & Wilson, 1967; MacArthur et al., 1972; avian speciation is the Zosterops white-eyes. Zosterops Diamond, 1974, 1998; Diamond et al., 1976). This have a wide distribution across the Indo-Pacific, South region is home to thousands of islands and several Asia and Africa (Van Balen, 2008). They are supreme widespread species radiations, perfect for studying island colonizers, which are found throughout the evolution in multiple, closely related populations Indo-Pacific, with 73 of the 96 currently recognized (Mayr & Diamond, 2001). Modern molecular tools have bolstered this work, uncovering cryptic Zosterops species being found on islands in this region (Mees, 1961, 1969; Mayr & Diamond, 2001; Warren et al., 2006; Van Balen, 2018a). Zosterops show one of *Corresponding author. E-mail: [email protected] the fastest speciation rates of any vertebrate (Moyle © 2019 The Linnean Society of London, Zoological Journal of the Linnean Society, 2019, XX, 1–24 1 2 D. P. O’CONNELL ET AL. Downloaded from https://academic.oup.com/zoolinnean/advance-article-abstract/doi/10.1093/zoolinnean/zlz022/5477306 by University College Dublin, [email protected] on 24 April 2019 et al., 2009), rivalled only by cichlid fish (Meyer, 1993; the molecular markers, in isolated populations, would Genner et al., 2007; Elmer et al., 2010). This rapid rate give greater insight into this rapidly evolving lineage of diversification has earned them the label as one of (Jønsson et al., 2014) and provide more effective the ‘great speciators’ of the Indo-Pacific, species groups species delimitation (Dong et al., 2015; Liu et al., 2016; marked out by their remarkable speciation rates Wood et al., 2016). (Mayr & Diamond, 2001; Moyle et al., 2009; Cornetti In the heart of the Wallacea region, the south- et al., 2015; Lim et al., 2018). eastern peninsula of Sulawesi provides an excellent Zosterops species embody the paradox of ‘great study system to test the effect of isolation on Zosterops speciators’ (Diamond et al., 1976): how do taxa that species (Fig. 1). There are continental islands (Buton, are sufficiently vagile to be such successful island Muna, Kabaena and Wawonii), which were connected colonizers become isolated and diverge into endemic to Sulawesi at the time of the last glacial maximum, species? Diamond et al. (1976) proposed that this around 20 000 years ago (Voris, 2000; Yokoyama pattern may arise from rapid shifts in dispersal et al., 2000; Clark et al., 2009), and oceanic islands ability in populations. The phylogeographic pattern (the Wakatobi Islands and Runduma Island), which of Zosterops species in Moyle et al. (2009) appeared have never been connected to the Sulawesi mainland consistent with this thesis. Dispersal ability can (Milsom & Ali, 1999; Nugraha & Hall, 2018). The be reduced in island taxa when adaptation to local region has been fruitful for recent speciation research. conditions favours traits other than dispersal ability While the Wakatobi Islands are only separated from (Mayr & Diamond, 2001; Gillespie et al., 2012). Buton by 27 km, they are home to six endemic bird Wright et al. (2016) assessed this phenomenon across subspecies (Kelly & Marples, 2010; Collar & Marsden, nine avian families (including the Zosteropidae) and 2014), a proposed new species of flowerpecker (Aves: found that reduced dispersal ability was associated Dicaeidae; Kelly et al., 2014) potential new subspecies with the lower species richness of predators on small of kingfisher (Aves: Alcedinidae; O’Connell et al., 2019). islands. Additionally, the phenomenon of ‘behavioural Kabaena Island, only 16 km from the mainland, is also flightlessness’, where isolated populations show home to an endemic subspecies of red-backed thrush, reduced propensity to fly across water barriers despite Geokichla erythronota subsp. kabaena (Robinson-Dean being physically capable of doing so, has been observed et al., 2002). to have evolved in multiple island bird and butterfly Current taxonomy identifies two Zosterops species, populations (Diamond, 1972, 1981; Holloway, 1977; the lemon-bellied white-eye, Zosterops chloris Diamond & Gilpin, 1983). Adaptations in island (Bonaparte, 1850), and the pale-bellied white-eye, populations that reduce the tendency to make long Zosterops consobrinorum (Meyer, 1904), in south-east flights may conserve energy in resource-constrained Sulawesi (Van Balen, 2018a). The natural history of islands (Diamond, 1981, 1984). these species is still being studied. Zosterops chloris The Zosterops radiation includes extremely is thought to be a typical ‘supertramp’ species (Mayr widespread species, such as the Japanese white-eye, & Diamond, 2001; Eaton et al., 2016). The designation Zosterops japonicus (Temminck & Schlegel, 1845), ‘supertramp’ was developed by Diamond (1974, 1975) and the Oriental white-eye, Zosterops palpebrosus to describe the island-colonizing behaviour of birds; (Temminck, 1824), containing multiple well-defined it includes the categories: (1) ‘sedentary’ – species races (Lim et al., 2018), ‘supertramp’ edge species such confined to the larger islands, (2) ‘tramps’ – present as the Louisiade white-eye Zosterops griseotinctus on larger islands but also many smaller and more (Gray, 1858), which are found on many small islands, remote islands and (3) ‘supertramps’ species that varying little throughout their range (Mayr & are confined as residents mainly to small islands Diamond, 2001), and a large number of single island and virtually absent from larger islands, apart from endemics (Van Balen, 2008). Recent molecular work edge habitats, such as mangroves, where they avoid has begun to re-draw the taxonomy and evolutionary stronger competitors. Zosterops chloris is found on relationships of widespread Zosterops species (Habel small islands from the east coast of Sumatra to the et al., 2013, 2015a; Cox et al., 2014; Husemann et al., west coast of Papua, and in coastal areas and edge 2015; Round et al., 2017; Wells, 2017; Lim et al., 2018) habitats on larger islands in the Lesser Sundas and even show unexpected divergence in supposedly and on Sulawesi, showing the habitat associations ‘supertramp’ lineages like Z. griseotinctus (Linck et al.,
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