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Downloaded from on 28 February 2019 Kent Academic Repository Full text document (pdf) Citation for published version van de Crommenacker, Janske and Bunbury, Nancy and Jackson, Hazel A. and Nupen, Lisa J. and Wanless, Ross and Fleischer-Dogley, Frauke and Groombridge, Jim J. and Warren, Ben H. (2019) Rapid loss of flight in the Aldabra white-throated rail. PLoS ONE . ISSN 1932-6203. (In press) DOI Link to record in KAR https://kar.kent.ac.uk/79029/ Document Version Author's Accepted Manuscript Copyright & reuse Content in the Kent Academic Repository is made available for research purposes. Unless otherwise stated all content is protected by copyright and in the absence of an open licence (eg Creative Commons), permissions for further reuse of content should be sought from the publisher, author or other copyright holder. Versions of research The version in the Kent Academic Repository may differ from the final published version. Users are advised to check http://kar.kent.ac.uk for the status of the paper. Users should always cite the published version of record. Enquiries For any further enquiries regarding the licence status of this document, please contact: [email protected] If you believe this document infringes copyright then please contact the KAR admin team with the take-down information provided at http://kar.kent.ac.uk/contact.html 1 Rapid loss of flight in the Aldabra white-throated rail 2 Janske van de Crommenacker1,2*, Nancy Bunbury1,3, Hazel A. Jackson2, Lisa J. Nupen4, Ross 3 Wanless4,5, Frauke Fleischer-Dogley1, Jim J. Groombridge2,† & Ben H. Warren6,† 4 5 1 Seychelles Islands Foundation (SIF), La Ciotat Building, PO Box 853, Mont Fleuri, 6 Victoria, Mahé, Seychelles 7 2 Durrell Institute of Conservation and Ecology (DICE), School of Anthropology and 8 Conservation, University of Kent, Marlowe Building, Canterbury, Kent CT2 7NR, UK 9 3 Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Penryn, 10 TR10 9FE, UK 11 4 DST/NRF Centre of Excellence at the Percy FitzPatrick Institute of African Ornithology, 12 University of Cape Town, Rondebosch 7701, Cape Town, South Africa 13 5 Institute of Marine Affairs and Resources Management, National Taiwan Ocean University, 14 Keelung, Taiwan 15 6 Institut de Systématique, Evolution, Biodiversité (ISYEB), UMR 7205 CNRS MNHN 16 UPMC EPHE UA, Muséum National d'Histoire Naturelle, Sorbonne Universités, 57 Rue 17 Cuvier, 75005 Paris, France 18 19 * Corresponding author: [email protected] 20 † Jointly senior (last) author 21 22 Short title: Rapid evolution of flightlessness in the Aldabra rail 23 24 Abstract 25 Flight loss has evolved independently in numerous island bird lineages worldwide, and 26 particularly in rails (Rallidae). The Aldabra white-throated rail (Dryolimnas [cuvieri] 27 aldabranus) is the last surviving flightless bird in the western Indian Ocean, and the only 28 living flightless subspecies within Dryolimnas cuvieri, which is otherwise volant across its 29 extant range. Such a difference in flight capacity among populations of a single species is 30 unusual, and could be due to rapid evolution of flight loss, or greater evolutionary divergence 31 than can readily be detected by traditional taxonomic approaches. Here we used genetic and 32 morphological analyses to investigate evolutionary trajectories of living and extinct 33 Dryolimnas cuvieri subspecies. Our data places D. [c.] aldabranus among the most rapid 34 documented avian flight loss cases (within an estimated maximum of 80,000–130,000 years). 35 However, the unusual intraspecific variability in flight capacity within D. cuvieri is best 36 explained by levels of genetic divergence, which exceed those documented between other 37 volant taxa versus flightless close relatives, all of which have full species status. Our results 38 also support consideration of Dryolimnas [cuvieri] aldabranus as sufficiently evolutionary 39 distinct from D. c. cuvieri to warrant management as an evolutionary significant unit. Trait 40 variability among closely related lineages should be considered when assessing conservation 41 status, particularly for traits known to influence vulnerability to extinction (e.g. 42 flightlessness). 43 44 Key words 45 Aldabra Atoll, evolutionary significant unit, extinction, rapid evolution of flightlessness, 46 isolated island population, Rallidae, taxonomic status 47 48 Introduction 49 Organisms living in island environments frequently undergo remarkable evolutionary changes 50 [1–4]. One such change is loss of flight, which has occurred worldwide in 26 bird families 51 from 17 orders [5]. Flight enables organisms to disperse, escape from predators and forage 52 [e.g., 6,7]. Species-poor islands that naturally lack mammal and bird predators have been 53 important in the evolution of flightlessness [8,9]. Consequently, loss of flight has evolved 54 independently in many insular bird species worldwide. Despite the high incidence of avian 55 flight loss on islands [9], the pace of evolutionary transitions underlying this trait is poorly 56 known. This is at least partly due to the fact that many insular flightless or poorly volant bird 57 species are extinct, and the scarcity of cases [11,12,13] in which there exist gradations in 58 flightlessness among or within extant lineages. 59 The avian family with the highest incidence of flight loss worldwide is the Rallidae 60 (rails; Order Gruiformes), with over 25% of the extant rail species being flightless [13]. The 61 family includes an estimated 135–150 extant species, plus numerous extinct forms [14], with 62 a global distribution that includes many oceanic islands, and a high proportion of island 63 endemics [15]. 64 Flightlessness has contributed to high extinction rates of island birds in the last 50,000 65 years, primarily driven by human colonization and the concomitant introduction of non-native 66 predators [16]. Rallidae have probably been the most susceptible avian family in this regard. 67 At least 65 species of Rallidae worldwide are documented as late Quaternary extinctions 68 [17,18] and another 35 species as recent extinctions (since ca . 1500 years BP). However, it is 69 estimated that such documented cases are greatly outnumbered by undocumented human- 70 induced rail extinctions, which may total 2000 species in the Pacific islands alone [16,19]. 71 Appropriate conservation assessment and protection of the remaining flightless Rallidae and 72 other avian species is therefore vital. 73 Our research focuses on the last surviving flightless bird in the biodiversity hotspot of 74 the Western Indian Ocean [20,21]: the Aldabra white-throated rail ( Dryolimnas [cuvieri ] 75 aldabranus ), which occurs only on Aldabra Atoll in the southern Seychelles. Historically, D. 76 cuvieri occurred on all four islands of the Aldabra group – Aldabra, Assumption (Fig 1), 77 Cosmoledo and Astove – before being extirpated from the latter three [10, 22–24]. There are 78 two other recognised subspecies: the volant Madagascar white-throated rail D. c. cuvieri , a 79 common endemic to Madagascar [10,22], and the extinct Assumption rail (D. c. abbotti ), 80 endemic to Assumption [25,26]. A second, extinct species of Dryolimnas , D. augusti , was 81 recently described based on fossil remains from Réunion Island [27], and a third species, 82 flightless and now extinct, once occurred on Mauritius [28,29]. Based on existing knowledge 83 and applying the common assumption that taxonomic status reflects genetic divergence, the 84 flightless Aldabra rail subspecies represents an enigma – it is flightless, yet only considered a 85 subspecies in an otherwise volant species. Therefore, either it would appear to be a candidate 86 for the youngest documented fully flightless bird lineage worldwide (and potential example of 87 such an evolutionary change being very rapid; [28]), or it is more divergent from the 88 Madagascar lineage than is readily inferred from current taxonomy. 89 Here we use genetic data from modern samples and museum specimens to examine 90 the phylogenetic placement of the flightless lineages of the Aldabra group, and investigate 91 whether or not their closest relative is indeed Dryolimnas of Madagascar. We further use 92 these data, in combination with morphological data from modern and museum samples, to 93 assess the degree of divergence of the flightless D. [c. ] aldabranus and the poorly volant D. c. 94 abbotti from the volant lineage of Madagascar. Genetic variation among populations of D. [c. ] 95 aldabranus is used to refine our understanding of important dispersal events in the 96 biogeographic history of this lineage. We also show how differentiation among D. [c. ] 97 aldabranus subpopulations can be used to inform effective management of this unique bird, 98 the last survivor among 12-17 flightless avian lineages that once occupied the Western Indian 99 Ocean region before human arrival [24]. 100 101 Materials and methods 102 Ethics statement 103 The ethical guidelines promoted by the Association for the Study of Animal Behaviour were 104 followed. Permission for sampling on Aldabra was issued by the Seychelles Islands 105 Foundation (local management authority), and the Department of Environment and the 106 Seychelles Bureau of Standards approved all research activities (approval reference A0347). 107 Sequences have been submitted to the NCBI GenBank (Accession Numbers: MH614934– 108 MH614960, MH645373–MH645415 and MH651394–MH651440). 109 110 Study site and species 111 The total population of D. [c. ] aldabranus occurs in an area of ca . 37.2 km 2, on the raised 112 atoll of Aldabra (152.6 km 2, 9°24' S, 46°20' E; Fig 1): with subpopulations on Picard (area: 113 9.4 km 2), Polymnie (1.9 km 2) and Malabar (25.9 km 2). A UNESCO World Heritage Site since 114 1982, Aldabra has been managed entirely for research and conservation since 1979 with only 115 a very small resident human population. 116 The Picard subpopulation of D. [c. ] aldabranus originates from a successful 117 reintroduction of 18 rails from Malabar in 1999 [30], after introduced feral cats on Picard 118 were removed by humans in the 1970s [30].
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