Genetic differentiation between migratory and sedentary populations of the Northern Boobook (Ninox japonica), with the discovery of a novel cryptic sedentary lineage Wen-Loung Lin, Lucia Liu Severinghaus, Hui-Yun Tseng & Si-Min Lin Journal of Ornithology ISSN 2193-7192 Volume 154 Number 4 J Ornithol (2013) 154:987-994 DOI 10.1007/s10336-013-0966-z 1 23 Your article is protected by copyright and all rights are held exclusively by Dt. Ornithologen-Gesellschaft e.V.. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy J Ornithol (2013) 154:987–994 DOI 10.1007/s10336-013-0966-z ORIGINAL ARTICLE Genetic differentiation between migratory and sedentary populations of the Northern Boobook (Ninox japonica), with the discovery of a novel cryptic sedentary lineage Wen-Loung Lin • Lucia Liu Severinghaus • Hui-Yun Tseng • Si-Min Lin Received: 11 September 2012 / Revised: 6 April 2013 / Accepted: 6 May 2013 / Published online: 21 May 2013 Ó Dt. Ornithologen-Gesellschaft e.V. 2013 Abstract Species that exhibit intraspecific variation in samples including ascertained breeders, ascertained migratory behavior provide a valuable opportunity to study migrants, and topotypes of the sedentary N. j. totogo from the evolution of avian migration. The Northern Boobook Lanyu, we found a coexistence of two clades with a 1.72 % (Ninox japonica) has two subspecies in East Asia, one sequence divergence, and both clades were highly sup- sedentary (N. j. totogo) and one migratory (N. j. japonica). ported in phylogenetic analyses. The clade containing The validity and residential status of the two subspecies has ascertained breeders occurs year round in Taiwan and is the never been examined through genetic analysis. Their only resident population during the breeding season. The coexistence in Taiwan provides an excellent opportunity to other clade containing ascertained migrants appears only in explore their genetic differentiation and migratory behav- non-breeding seasons and coexists with the former during ior. Analyzing the mitochondrial cytochrome b gene of 77 these months. Topotypes of N. j. totogo from Lanyu were clustered with N. j. japonica, which undermines its clas- sification as a subspecies. We suggest treating N. j. totogo Communicated by M. Wink. as an invalid taxon and treating the sedentary population in Electronic supplementary material The online version of this Taiwan as a unique cryptic lineage until further informa- article (doi:10.1007/s10336-013-0966-z) contains supplementary tion is available. The discovery of this lineage will improve material, which is available to authorized users. our understanding of the owls in terms of animal conser- vation, genetic biodiversity, and the evolution of their W.-L. Lin Á S.-M. Lin (&) Department of Life Science, National Taiwan Normal migratory behavior. University, Taipei City, Taiwan e-mail: fi[email protected] Keywords Cryptic species Á Genetic diversity Á Migration route Á Orchid Island Á Rescue center Á W.-L. Lin Taichung Wildlife Conservation Group, Taichung, Taiwan Sympatric distribution L. L. Severinghaus Zusammenfassung Biodiversity Research Center, Academia Sinica, Taipei City, Taiwan Genetische Unterscheidung von Standvo¨gel- und Zu- L. L. Severinghaus Á S.-M. Lin gvo¨gel-Populationen des No¨rdlichen Boobookkauz (Ni- Raptor Research Group of Taiwan, Taipei City, Taiwan nox japonica; Strigidae) im Zusammenhang mit dem Fund einer neuen, noch ungekla¨rten ortsabha¨ngigen H.-Y. Tseng (&) Zoology Department, National Museum of Natural Science, Abstammungslinie Taichung, Taiwan e-mail: [email protected] Arten mit innerartlich unterschiedlichem Zugverhalten bieten eine wichtige Mo¨glichkeit, die Entstehung des H.-Y. Tseng Department of Life Science, Tunghai University, Taichung, Vogelzugs zu untersuchen. Der No¨rdliche Boobookkauz Taiwan (Ninox japonica) kommt in Ostasien in zwei Unterarten 123 Author's personal copy 988 J Ornithol (2013) 154:987–994 vor; die Tiere der einen (N. j. totogo) sind reine Standvo¨gel, die der anderen (N. j. japonica) sind Zugvo¨gel. Bislang ist die Validita¨t dieser Feststellung zu Stand- versus Zugvogel aber nie anhand einer genetischen Analyse u¨berpru¨ft wor- den. Das gleichzeitige Vorkommen beider Unterarten in Taiwan bietet eine ausgezeichnete Mo¨glichkeit, ihr Zug- verhalten und ihre genetischen Unterschiede zu untersuchen. Bei der Analyse des mitochondrialen Cytochrome b-Gens aus 77 Proben u.a. von eindeutig nachgewiesenen Stand- vo¨geln, Zugvo¨geln und Topotypen der nicht ziehenden Unterart N. j. totogo von der Insel Lanyu (vor der su¨do¨stli- chen Ku¨ste Taiwans) fanden wir ein gemeinsames Auftreten von zwei Gruppen mit einer Sequenz-Abweichung von Fig. 1 A Northern Boobook (Ninox japonica) flying across the 1.72 %, wobei das Vorhandensein beider Gruppen auch ocean between Taiwan and Lanyu. This picture provides evidence for phylogenetisch hoch absicherbar war. Die Gruppe mit den the oversea dispersal of this species, and might be one of the very few nachgewiesenen Standvo¨geln kann das ganze Jahr u¨ber in photographic records of a subtropical forest owl on migration. Taiwan angetroffen werden und ist wa¨hrend der Brutzeit die Photographed by Mei-Fong Liao from a boat at 14:53 hours, April 19, 2012 einzige dort vorhandene Population. Die andere Gruppe mit den Ziehern kommt dort nur außerhalb der Brutzeiten und dann gemeinsam mit der ersten Gruppe vor. Die Topotypen the species diversity of some sedentary lineages is still von N. j. totogo von Lanyu wurden mit N. j. japonica zu- underestimated (e.g., the recent discovery of N. rumseyi and sammengefasst, was ihre Klassifizierung als eigene Unterart N. leventisi by Rasmussen et al. 2012). Variation in migra- untergra¨bt. Wir regen an, bis zum Vorliegen weiterer In- tory status also occurs at the conspecific level in some cases, formationen N. j. totogo als ungu¨ltiges Taxon anzusehen und such as in the N. japonica discussed in this study (Ko¨nig die Standvo¨gel-Population in Taiwan als eigene, noch nicht et al. 2009). The Taiwan population was initially regarded as ganz gekla¨rte Abstammungslinie zu betrachten. Die Ent- a migrant (Hachisuka and Udagawa 1951), then changed to deckung dieser Linie wird unser Versta¨ndnis der Eulen im a resident based on its year-round presence (Mees 1970; Zusammenhang mit Artenschutz, genetischer Vielfalt und King 2002; Dickinson 2003), and recently with more der Entstehung ihres Zugverhaltens verbessern. information reclassified as containing both sedentary and migratory elements (Brazil 2009; Severinghaus et al. 2010). N. japonica (Temminck and Schlegel 1845) was previ- ously classified as a subspecies of N. scutulata (Raffles Introduction 1822), i.e. N. scutulata japonica, and subsequently elevated to species (King 2002) based on its diagnostic vocal char- The evolution of genetic and phenotypic traits in migratory acters. According to the revised species definition, N. birds has attracted much attention of ornithologists in japonica has a distribution covering southeastern Siberia, recent years (Webster et al. 2002; Cotton 2003; Liedvogel Korea Peninsula, northeastern and central China, Japan, et al. 2011). Active areas of inquiry include investigations Taiwan, and Lanyu (Brazil 2009). King (2002) separated the of the time needed for migratory behavior to arise, or the species into two subspecies: N. j. totogo Momiyama 1930 genetic differentiation between closely related lineages distributed in Taiwan and Ryukyu Islands with type locality representing different migratory phenomena (Pe´rez-Tris in Lanyu (an island located approximately 60 km to the et al. 2004; Bearhop et al. 2005; Rolshausen et al. 2009; southeast of Taiwan); and N. j. japonica distributed in the Bensch et al. 2009). Separate lineages can evolve in allo- rest of the species’ range. Brazil (2009) treated breeders in patric breeding sites and meet at wintering sites, or be Korea and Japan as N. j. japonica, while breeders in Taiwan, sympatrically distributed but with different migratory Lanyu, and southern Ryukyus as N. j. totogo (Fig. 2a). routes (Bearhop et al. 2005; Bensch et al. 2009; Rolshausen Breeding of N. japonica in Taiwan was not formally et al. 2009). The genetic differentiation between such lin- described until 2012 (Lin et al. 2012), while breeding of N. j. eages provides a valuable opportunity to examine the totogo in Lanyu has been known for some time (Severing- development of migratory behaviors. haus et al. 2010). However, validity and residential status of Ninox, also known as Hawk Owls or Boobooks, is an owl these two taxa have never been discussed. genus with approximately 20 species distributed mainly in Analyzing genetic diversity can provide useful insight into Australia and Asia (Ko¨nig et al. 2009). Members of this population structure. According to current classification, there genus do not have uniform migratory behavior (Fig. 1), and should be only one taxon occurring Taiwan in the breeding 123 Author's personal copy J Ornithol (2013) 154:987–994 989 A C 2 N. j. japonica N. j. totogo Taiwan B 56 7 N. j. japonica N. j. japonica Lanyu Is. 1 N. j. totogo N. japonica ssp. Penghu Is. 9 Breeders in Taiwan Status unknown N. j. japonica Fig. 2 a The taxonomy of Northern Boobook (Ninox japonica)as population in Taiwan. c Sampling location and sample size used in shown in the literature contains a migratory population (N. j. this study. The ascertained status of the samples were based on japonica) and a sedentary population (N.