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Conservation Genetics of the Bengal Tiger (Panthera Tigris Tigris) in India

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Conservation Genetics of the Bengal Tiger (Panthera Tigris Tigris) in India A 689 OULU 2017 A 689 UNIVERSITY OF OULU P.O. Box 8000 FI-90014 UNIVERSITY OF OULU FINLAND ACTA UNIVERSITATISUNIVERSITATIS OULUENSISOULUENSIS ACTA UNIVERSITATIS OULUENSIS ACTAACTA SCIENTIAESCIENTIAEA A RERUMRERUM Sujeet Kumar Singh NATURALIUMNATURALIUM Sujeet Kumar Singh Sujeet Kumar University Lecturer Tuomo Glumoff CONSERVATION GENETICS University Lecturer Santeri Palviainen OF THE BENGAL TIGER Postdoctoral research fellow Sanna Taskila (PANTHERA TIGRIS TIGRIS) IN INDIA Professor Olli Vuolteenaho University Lecturer Veli-Matti Ulvinen Planning Director Pertti Tikkanen Professor Jari Juga University Lecturer Anu Soikkeli Professor Olli Vuolteenaho UNIVERSITY OF OULU GRADUATE SCHOOL; UNIVERSITY OF OULU, FACULTY OF SCIENCE; Publications Editor Kirsti Nurkkala WILDLIFE INSTITUTE OF INDIA ISBN 978-952-62-1565-5 (Paperback) ISBN 978-952-62-1566-2 (PDF) ISSN 0355-3191 (Print) ISSN 1796-220X (Online) ACTA UNIVERSITATIS OULUENSIS A Scientiae Rerum Naturalium 689 SUJEET KUMAR SINGH CONSERVATION GENETICS OF THE BENGAL TIGER (PANTHERA TIGRIS TIGRIS) IN INDIA Academic dissertation to be presented with the assent of the Doctoral Training Committee of Health and Biosciences of the University of Oulu for public defence in the Arina auditorium (TA105), Linnanmaa, on 19 May 2017, at 12 noon UNIVERSITY OF OULU, OULU 2017 Copyright © 2017 Acta Univ. Oul. A 689, 2017 Supervised by Professor Jouni Aspi Docent Laura Kvist Doctor Surendra Prakash Goyal Reviewed by Professor Gernot Segelbacher Docent Perttu Seppä Opponent Professor Pekka Pamilo ISBN 978-952-62-1565-5 (Paperback) ISBN 978-952-62-1566-2 (PDF) ISSN 0355-3191 (Printed) ISSN 1796-220X (Online) Cover Design Raimo Ahonen JUVENES PRINT TAMPERE 2017 Singh, Sujeet Kumar, Conservation genetics of the Bengal tiger (Panthera tigris tigris) in India. University of Oulu Graduate School; University of Oulu, Faculty of Science; Wildlife Institute of India Acta Univ. Oul. A 689, 2017 University of Oulu, P.O. Box 8000, FI-90014 University of Oulu, Finland Abstract Tigers are endangered in the wild and face increasing threats from habitat loss and fragmentation. The majority of their range occurs in the Indian subcontinent, which is therefore a critical area for tiger conservation. Bengal tigers are distributed across many small protected areas in India. Two important Bengal tiger landscapes – Terai Arc Landscape (TAL) and Sundarbans in India were lacking in basic genetic information and needed to address the impact of anthropogenic pressure and climate change on their genetic makeup in order to identify conservation units. Therefore, I employed nuclear and mitochondrial genetic markers on TAL and Sundarbans tiger individuals to respond these demands for the first time. Thirty-nine heterologous microsatellite loci were screened on Bengal tigers and thirteen of these loci were selected to genotype Bengal tiger samples from western TAL (WTAL) and Sundarbans. After I had genotyped seventy-one Bengal tiger individuals from WTAL, I found cryptic population genetic structure, moderate gene flow and asymmetric migration among the subpopulation. Genetic diversity was moderate and there were no signs of population bottlenecks. In order to maintain the connectivity of subpopulations and avoid human–wildlife conflict, relocation of villages is necessary. Preventive measures against habitat encroachment and a ban on sand and boulder mining in the corridor area should also be implemented. Noninvasively-collected tiger samples from Sundarbans were analyzed for mitochondrial and microsatellite markers and compared with mainland (northern and peninsular) Bengal tiger populations in India. Sundarbans tigers were found to be genetically distinct and had lower genetic variation in comparison to other mainland tiger populations. Demographic analysis indicated recent historical isolation (600–2000 years ago) of the Sundarbans tiger from the mainland. Both historical and genetic evidence supported that the Sundarbans tiger was genetically connected to other mainland tigers until recently. Conclusively, genetic isolation from the mainland tiger population and adaptation to the mangrove ecosystem might have jointly shaped the genetic architecture of the Sundarbans tiger. Hence, the Sundarbans tiger needs special conservation attention for the preservation of its unique ability to adapt and for its genetic individuality. It should be managed as an evolutionary significant unit (ESU) under the adaptive evolutionary conservation (AEC) criteria. I also addressed a problem in the previously suggested sex-specific gene flow estimation method and recommended an alternative approach for a more precise estimation. Keywords: anthropogenic pressure, conservation unit, population genetic structure, Sundarbans, Terai Arc Landscape Singh, Sujeet Kumar, Intiantiikerin (Panthera tigris tigris) luonnonsuojelu- genetiikka. Oulun yliopiston tutkijakoulu; Oulun yliopisto, Luonnontieteellinen tiedekunta; Wildlife Institute of India Acta Univ. Oul. A 689, 2017, Oulun yliopisto, PL 8000, 90014 Oulun yliopisto Tiivistelmä Tiikeri on nykyisin uhanalainen lajin elinympäristön supistumisen ja pilkkoutumisen vuoksi. Lajin tärkein esiintymisalue on Intian niemimaalla, joka on siten kriittisen tärkeä alue tiikerin suojelun kannalta. Intiantiikereitä esiintyy useilla pienillä suojelualueilla Intiassa. Kaksi tärkeää tiikerin esiintymisaluetta Intiassa ovat Terain kaaren (TAL) alue luoteis-Intiassa sekä Sundarban- sin mangrovealue Bangladeshin rajalla. Näiden alueiden tiikereistä ei ole ollut olemassa geneet- tistä perustietoutta, jota tarvitaan, kun arvioidaan ihmisen toiminnan ja ilmastonmuutoksen aihe- uttamia muutoksia tiikeripopulaatioiden geneettisessä koostumuksessa sekä kun määritellään lajin suojelun kannalta merkittäviä luonnonsuojeluyksikköjä. Tässä väitöskirjatutkimuksessa tut- kittiin Terain kaaren ja Sundarbansin alueen tiikereiden geneettistä monimuotoisuutta ja raken- netta sekä tuman että mitokondrion geenimerkkien avulla. Tutkimuksessa selvitettiin kolmen- kymmenyhdeksän tuman geenimerkin (mikrosatelliitin) soveltuvuutta intiantiikerin geneettisiin tutkimuksiin, ja näistä valittiin kolmetoista käytettäväksi läntisen Terain kaaren ja Sundarbansin alueiden tiikereiden geneettisiin tutkimuksiin. Terain kaaren alueelta tutkittiin seitsemänkymme- nentäyksi intiantiikerinäytettä. Tulosten perusteella alueella on aikaisemmin havaitsematonta kryptistä populaatiorakennetta. Geenivirtaa eri alapopulaatioiden välillä oli kohtuullisen paljon, mutta se oli epäsymmetristä. Tiikereiden geneettinen monimuotoisuus oli melko suurta eikä geneettisillä menetelmillä havaittu eri alapopulaatioissa merkkejä populaation koon pullonkau- loista. Jotta alapopulaatioiden välinen yhdistyneisyys säilyisi jatkossa, joidenkin kylien siirto toisaalle on välttämätöntä. Ihmisten luvaton levittäytyminen tiikerin elinalueita yhdistävillä käy- tävillä täytyisi saada hallintaan sekä kieltää hiekanotto ja kivenlouhinta. Sundarbansin alueelta ei-invasiivisesti kerätyt tiikerinäytteet tutkittiin sekä tuman että mitokondrion merkkigeenillä ja alueen tiikereiden geneettistä koostumusta verrattiin manner-Intian tiikeripopulaatioiden koostu- mukseen. Sundarbansin tiikereiden todettiin poikkeavan geneettisesti manneralueen tiikeripopu- laatioista ja niiden geneettinen monimuotoisuus oli alhaisempaa kuin manneralueella. Koale- senssisimulaatiohin perustava demografinen analyysi viittasi Sundarbansin tiikereiden suhteelli- sen viimeaikaiseen (600–2000 vuotta sitten) erkanemiseen manneralueen tiikereistä. Sekä histo- rialliset että geneettiset todisteet tukivat teoriaa, jonka mukaan Sundarbansin tiikereillä olisi ollut yhteyksiä mannermaan tiikereihin aivan viime aikoihin asti. Geneettinen isolaatio manner- maan tiikereistä ja adaptaatio mangrove-ekosysteemiin ovat yhdessä muovanneet Sundarbansin tiikereiden geneettistä arkkitehtuuria. Tämän vuoksi Sundarbansin tiikerit vaativat erityistä suo- jelua, jotta niiden geneettinen ainutlaatuisuus ja kyky sopeutua erityisolosuhteisiin säilyisivät myös tulevaisuudessa. Populaatiota täytyy hoitaa evolutiivisesti merkittävänä yksikkönä (evolu- tionary significant unit; ESU) adaptiivisen evolutiivisen suojelun (adaptive evolutionary conser- vation; AEC) kriteeristön mukaisesti. Tutkimuksessa kiinnitettiin huomiota myös ongelmiin, joi- ta saattoi ilmetä aikaisemmin ehdotetuissa menetelmissä eri sukupuolten kautta kulkevan geeni- virran määrän arvioimiseksi ja ehdotettiin vaihtoehtoista menetelmää tarkempien arvioiden saa- miseksi. Asiasanat: ihmisen vaikutus, luonnonsuojeluyksikkö, populaatiogeneettinen rakenne, Sundarbans, Terain kaari Dedicated to my parents and family 8 Acknowledgements This thesis signifies not only my work at the keyboard, but it is also an achievement of my more than six years of continuous effort at University of Oulu and Wildlife Institute of India. It would not have been possible without the guidance and support of several peoples who directly or indirectly contributed and extended their valuable support in the preparation and completion of this study. I would like to express my sincere gratitude to all of them. First and foremost, I would like to express my sincere gratitude to my doctoral supervisors Prof. Jouni Aspi, Dr. S.P. Goyal and Doc. Laura Kvist for their exceptional supervision, care, forbearance, and for providing me with an excellent atmosphere for conducting research. I will never forget the teachings of Dr. S.P. Goyal. I remember very well when I started working with Dr. Goyal in the Wildlife Forensic
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