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Diversification of A Ibis (2018) doi: 10.1111/ibi.12688 Diversification of a ‘great speciator’ in the Wallacea region: differing responses of closely related resident and migratory kingfisher species (Aves: Alcedinidae: Todiramphus) DARREN P. O’CONNELL,1,2* DAVID J. KELLY,1,2 NAOMI LAWLESS,1,2 ADI KARYA,3 KANGKUSO ANALUDDIN3 & NICOLA M. MARPLES1,2 1Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin DO2 CX56, Ireland 2Trinity Centre for Biodiversity Research, Trinity College Dublin, Dublin DO2 CX56, Ireland 3Department of Biology and Biotechnology, Universitas Halu Oleo, Kendari, Southeast Sulawesi, Indonesia The Collared Kingfisher species complex is the most widespread of the ‘great speciator’ lineages of the Indo-Pacific. They have shown a remarkable ability to spread and diversify. As a result of this rapid diversification, Todiramphus species are often found in secondary sympatry. In Southeast Sulawesi, Indonesia, two Todiramphus species are present, the breeding resident Collared Kingfisher Todiramphus chloris and the overwintering migratory Sacred Kingfisher Todiramphus sanctus. We investigated the effect of isolation on these closely related species by comparing their populations on mainland Sulawesi and its larger continental islands, with populations on the small, oceanic Wakatobi Islands. Within our wider analysis we provide further support for the distinctiveness of the Sulawesi Collared Kingfisher population, perhaps isolated by the deep water barrier of Wallace’s line. Within Sulawesi we found that populations of Collared Kingfisher on the Wakatobi Islands had diverged from those on mainland Sulawesi, differing both in morphology and in mitochon- drial DNA. In contrast, there was no divergence between Sacred Kingfisher populations in either morphology or mitochondrial DNA. We propose that a difference in habitat occu- pied by Collared Kingfisher populations between the mainland and continental islands vs. oceanic islands has caused this divergence. Mainland Collared Kingfishers are predomi- nately found inland, whereas Wakatobi Collared Kingfishers are also found in coastal habi- tats. The larger body size of Wakatobi Collared Kingfisher populations may be a result of increased competition with predominantly coastal Sacred Kingfisher populations. The uni- form nature of Sacred Kingfisher populations in this region probably reflects their consis- tent habitat choice (coastal mangrove) and their migratory nature. The demands of their breeding range are likely to have an even stronger selective influence than their Sulawesi wintering range, limiting their scope for divergence. These results provide insight into the adaptability of the widespread Todiramphus lineage and are evidence of the need for fur- ther taxonomic revision of Collared Kingfisher populations. Keywords: competition, evolution, great speciator, Indo-Pacific, islands, kingfisher, Todiramphus, Wallacea. Island bird populations have historically been of biogeography (Darwin 1859, Wallace 1869). They great importance in the study of evolution and provide discrete units which provide insight into how species adapt and change in relative isolation (MacArthur & Wilson 1967, Whittaker & Fernan- *Corresponding author. dez-Palacios 2007). Modern molecular tools have Email: [email protected] provided new avenues for this research, allowing Twitter: @oconned5 © 2018 British Ornithologists’ Union 2 D. P. O’Connell et al. for both greater insight into the evolutionary his- (Andersen et al. 2015b), making it one of the fast- tory of the taxa (Jetz et al. 2012) and the discov- est diversifying lineages of birds (Moyle et al. ery of previously unrecognized ‘cryptic’ species 2009, Jetz et al. 2012). The colonization of ocea- (Bickford et al. 2007). The Indo-Pacific is of par- nic islands is thought to have played a major part ticular importance to this area of research. This in the extraordinary diversification of the Collared region has great potential for cryptic diversity Kingfisher species complex. The rapid diversifica- (Lohman et al. 2010) and its many islands make it tion seen in this group occurred when colonizing perfect for studying the tempo and mode of speci- the oceanic islands of Wallacea, the Philippines ation in birds. The Indo-Pacific is home to a num- and the Pacific (Andersen et al. 2018). ber of groups of birds known as ‘great speciators’ This ability to colonize islands has led to multi- (Diamond et al. 1976), taxa renowned for their ple instances of secondary sympatry, where two or large geographical ranges and rapid diversifications more recently diverged Todiramphus species are (Mayr & Diamond 2001). found on the same island (Woodall 2001). Such Mayr and Diamond (2001) developed the ‘great closely related species have similar ecological speciator’ concept for their study system in North- requirements so they might be expected to com- ern Melanesia to describe a group of birds with pete strongly for resources (MacArthur & Levins high inter-island geographical variation, including 1967, Martin & Martin 2001, Lovette & diverse taxa found across many islands (e.g. Louisi- Hochachka 2006). However, multiple coloniza- ade White-eye Zosterops griseotinctus, Moluccan tions of island archipelagos have occurred in many Dwarf Kingfisher Ceyx lepidus, Australian Golden taxa, with very different outcomes, depending on Whistler Pachycephala pectoralis and Common the traits of those taxa. For example, although Cicadabird Edolisoma tenuirostre). Because of their multiple colonizations of Pacific reed-warblers wide ranges and multiple distinct populations, the (Acrocephalus) occurred in three archipelagos, ‘great speciators’ have provided ideal study systems species from different lineages do not co-occur on for developing many key concepts in evolutionary any island (Cibois et al. 2011). Reed-warblers live biology (Mayr 1942, Diamond 1974, Diamond in high-density populations of territorial pairs and et al. 1976). In recent years modern molecular trios, potentially saturating available habitat and methods have enabled researchers to begin to preventing the establishment of new immigrants uncover the intricate evolutionary histories of the (Craig 1992, Graves 1992, Thibault & Cibois ‘great speciators’, showing them to be complexes 2006). In contrast, two species of white-eye (Zos- of closely related species (Andersen et al. 2013, teropidae) coexist on several Mariana Islands (Sli- 2014, Irestedt et al. 2013, Pedersen et al. 2018). kas et al. 2000), probably aided by the social The Collared Kingfisher Todiramphus chloris flocking behaviour of white-eyes (van Balen 2008). species complex is one of the most widespread of The phenomenon of multiple colonizations of the ‘great speciator’ lineages of the Indo-Pacific, island archipelagos is perhaps best studied in the covering over 16 000 km from the Red Sea to Indian Ocean archipelago, a diverse collection of Polynesia (Woodall 2001, Andersen et al. 2015b). islands in terms of both island area and ecology This species complex shows great diversification (Whittaker & Fernandez-Palacios 2007). White- across its wide range, encompassing the Collared eyes and sunbirds (Nectarinia) show a complex Kingfisher (14 subspecies) and five species recently pattern of island occupancy in the Indian Ocean taxonomically split from the Collared Kingfisher in archipelago. Most islands are home to only one the IOC World Bird List (v. 8.1), based on work species from each genus and competition with by Andersen et al. (2015b): the Torresian King- congeneric species limits the further diversification fisher Todiramphus sordidus (three subspecies), of colonists (Warren et al. 2003, 2006). There are Islet Kingfisher Todiramphus colonus (monotypic), only a few exceptions. White-eye species live in Mariana Kingfisher Todiramphus albicilla (three sympatry on only three Indian Ocean islands, seg- subspecies), Melanesian Kingfisher Todiramphus regated according to altitude (Warren et al. 2006). tristrami (seven subspecies) and Pacific Kingfisher Sunbirds are also only found in sympatry on three (22 subspecies) (Gill & Donsker 2018). This level islands, partitioned by morphological niche (Bij- of diversification is particularly remarkable given nens et al. 1987). Sunbirds are even excluded from that the Collared Kingfisher species complex La Reunion and Mauritius by the endemic white- started diversifying within the last 0.57–0.85 Ma eyes (Reunion Olive White-eye Zosterops olivaceus © 2018 British Ornithologists’ Union Diversification of a Wallacean ‘great speciator’ 3 and Mauritius Olive White-eye Zosterops chloro- significantly revised the taxonomy of this remark- nothos respectively), which have abnormally long able diversification, the morphological and ecologi- bills for white-eyes and fill the sunbird niche (Gill cal adaptations that led to the isolation of the 1971, Cheke 1987). Clearly, interactions with tax- different populations remain to be studied. While onomically and ecologically similar species, as well morphology and phylogenetics have co-varied in as island characteristics, are important for the many taxa (Jablonski & Finarelli 2009, McKay spread of island-colonizing species (Franzen et al. et al. 2010, Dong et al. 2015, Liu et al. 2016) 2012). there are multiple examples of differing morpho- Todiramphus populations in secondary sympatry logical and phylogenetic patterns, particularly in have been shown to exhibit separation by habitat recently diverged island fauna (Cibois et al. 2007, preference, which allow these closely related spe- Phillimore et al. 2008, Saitoh
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