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MOLECULAR Systematlcs of NEOTROPICAL DEER MICE of the PEROMYSCUS UEXTCAVUS SPECIES GROUP

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MOLECULAR SYSTEMATlCS OF NEOTROPICAL DEER MICE OF THE PEROMYSCUS UEXTCAVUS SPECIES GROUP Nicola Lourdes Wade A thesis submitted in conformity with the requirements for the degree of Master of Science Graduate Department of Zoology University of Toronto O Copyright by Nicola Lourdes Wade 1999 National Library Bibl'ithèque nationale du Canada Acquisitions and Acquisitions et Bibliographie Services sentices bibliographiques 395 Wellington Street 395. rue Weilingtori Ottawa ON KlA ON4 OttawaON KIAW Canada Canada The author has granted a non- L'auteur a accordé une licence non exclusive Licence allowing the exclusive permettant à la National Library of Canada to Bibliothèque nationale du Canada de reproduce, loan, dismbute or sell reproduire, prêter, distribuer ou copies of this thesis in microform, vendre des copies de cette thèse sous paper or electronic formats. la forme de microfiche/nlm, de reproduction sur papier ou sur format électronique. The author retains ownership of the L'auteur conserve la propriété du copyright in this thesis. Neither the droit d'auteur qui protège cette thèse. thesis nor substantial extracts fkom it Ni la thèse ni des extraits substantiels may be printed or otherwise de celle-ci ne doivent être imphés reproduced without the author's ou autrement reproduits sans son permission. autorisation. ABSTRACT Molecular Systematics of Neotropical Deer Mice of the Peromysclrs mexicanus Species Group. 1999. Nicola Lourdes Wade. Graduate Department of Zoology, University of Toronto. Mitochondrial DNA sequences of cytochrorne b, M)3, ND4L, and ND4 were used as phylogenetic markers to re-examine the systematic arrangement of the P. rnexicanus species group. Phylogenetic relationships were estimated on the combined sequences using neighbour joining, weighted (6: 1) parsimony, and maximum likelihood rnethods. Contrasting phylogenetic hypotheses of Hooper and Musser (1964, as rnodified by Huckaby 1%O), and Carleton (1989) were tested. Phylogenetic analysis of the mtDNA data most closely approximates Hooper and Musser's (1 964) concept of the species group. Withh the 'core' rnexicanus group, P. mexicanur is not monophyletic, and is segregated into three phylogenetically distinct groups. The nucleotide sequence data supported the polyphyletic arrangement of P. nudipes, which may be a result of separate invasions fiom two different P. mexicanus popuIations. The phylogenetic relationships between the highland taxa including P. sarhynchus, P. guatemalensis, and P. grandis do not conform to any of Huckaby's (1 980) three hypotheses, merdemonstrating their complex geographical relationships. Phylogenetic evidence suggests that P. g~mnotisand membea of the western P. mexicanus lineage are conspecific. ACKNOWLEDGEMENTS 1 would like to thank Dr. Mark Engstrom my supervisor, for giving me the opportunity to study molecular systematics of deer mice, for funding the project, and editing my thesis under such time constraints. 1 wodd also like to thank hun for sharing with me his extensive knowledge in mammalogy, particularly with Peromysctts, and 1 appreciate his broad knowledge of Central America 1 would also Iike to thank Dr. Allan Baker my adjunct supervisor for his support, advice, and encouragement throughout the course of my degree. 1 thank him for allowing me to work in his lab and the use of his cornputers to perform my analysis (despite the immense cornpetition for computing time). A warm thank you to my family for their support and encouragement. Without them this thesis would not be possible. Special thanks goes to Oliver Haddrath for assisting me with getthg started in the lab, for showing me the 'ropes' ,and for his support, and advice. Oliver is one of the most patient, understanding, and kind people 1 have ever had the pleasure of knowing. His keen imagination always managed to amaze me; 1 have my lab bench to thank for that! (Oliver, the war is not over yet!). Another special thanks goes to my colleague and dearest fnend Tara Paton. Her fnendship and support has meant the world to me. 1 thank her for her assistance and constant advice during ail phases of my thesis. The two of us together made a great team, we conquered PAUP*! 1 hope 1 have the pleasure of working with her again in the future. iii I especially thank my additionai surrogate family fiom the lab who have made my graduate expenence exciting and fun. Maryann Burbidge, my bench partner, thank you for your help in the [ab, for your good advice, and your pep talks about 'the worst thhgs that could happen'. Many thanks to Andy Given for his fun little antics that managed to take the pressure off' I wouid like to express my gratitude to Mark Peck for his endless supply of patience and use of his computer, Dr- AIejandro Lynch for his computer advice, Burton Lim for his assistance with locating the Perornyscus samples and localities, and Amy Lathrop for her expertise and patience with my many parsimony-related questions. 1 would also like to thank the folîowing people for discussions: Dr. Jan Hughes, Dr. Alessandro Grapputo, Dr. Mike Dennison, Dr. John Barlow, and Annette Greendade. For their administrative assistance, 1 would like to thank Elizabeth Tudor- Mulroney and Susan Del Tufo fiom the Zoology Graduate Department, and Cathy Ayley from the ROM. This research was hded in part by a Natural Sciences and Engineering Research Council of Canada operating grant to Dr. M. D. Engstrom, the ROM foundation, Dr. M. D. Engstrom, and the field work fund fiom the Centre for Biodiversity and Conservation Biology at the ROM. 1 would also Iike to thank Ange10 State University (ASNHC); Institut0 de Biologia, Universidad Nacional Authorna de Mexico (IBUNAM); The Natural History Museum of Los Angeles County (LACM); Brigham Young University (BYU); University of Kansas, Museum of Natural History (KU); Cincinnati Museum of Natural History (CM); and the Royal Ontario Museum (ROM) for supplying tissue samples. TABLE OF CONTENTS .. ABSTRACT .......................................................................................... 11 ... ACKNO WLEDGEMENTS ....................... ... ........................................ ..LU TABLE OF CONTENTS .................... .... ....... ,.., ........................................ v .. LIST OF TABLES ......................................................... .........................vu LIST OF FIGURES ................................................................................. ix .. LIST OF APPENDICES ........................................................................... xu rNTRODUCTION .................................................................................... 1 MATERIALS AND METHODS ................................................................... 8 Tissues exarnined ...................................... ,............... -8 Molecular procedures ........................... .. ...................................... ..8 Sequence analysis ...................... ... .... ....................................... 12 Anal ytical methods .......... .. ......... .............. .. ................................ 13 Phylogenetic analysis ..................................................................... 16 RESULTS .................... ... .................................................................. 22 Gene characteristics .................... ... .......... .. .... ........ ..22 Gene Region Variability ................................................................. -35 Test for saturation ........................................................................ -38 Models of sequence evolution ............................... ............................ 38 Distance measures ........................................................................ -46 Rate variation among sites within genes ................................................ 47 Phy logenetic reconstruction ............................................................. -55 Conformance to previous systematic hypotheses ..................................... 68 DISCUSSION .................... ,.. ....... .,,, ...................................................73 Content of the Peromyscus mexicanus species group ................................ -73 Phylogenetic relationships among members of the P . mexicallus group ........... 74 Speciation within the 'core' mexicarms group ........................................ -75 SUMMARY .........................................................................................81 LITERATURE CITED ............................................................................ -83 APPENDICES ......................... ..............................................................93 LIST OF TABLES Table 1. An overview of the different hypotheses relationships in the Peromyscus mexiconus species group according to Osgood (1 909), Hooper and Musser (1964), Hooper (1968), and Carleton (1 989) ...................................... .3 Table 2. Sequence charactenstics for al1 four rnitochondrial genes among 20 species of the subgenus Peromysctls ............................................................ 23 Table 3. Average number of transitions and transversions for each of four mitochondrid genes in 20 species of the subgenus Peromyscus .............-25 Table 4. Percentage nucleotide composition for dl20 species of the subgenus Peromyscu~,excluding the outgroups Reithrodontomys, Boiomys, and Onychomys ............................................................................ -28 Table SA. Codon frequency for al1 20 species
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    PUBLICATIONS OF ROBERT D. BRADLEY 2019 190. Phillips, Caleb D., Jonathan L. Dunnam, Robert C. Dowler, Lisa C. Bradley, Heath Garner, Kathy McDonald, Burton K. Lim, Marcy A. Revelez, Mariel L. Campbell, Joseph A. Cook, Robert D. Bradley, and the Systematic Collections Committee of the American Society of Mammalogists. Curatorial guidelines and standards of the American Society of Mammalogists for collections of genetic resource. Journal of Mammalogy 100:1690- 1694. 189. Bradley, Robert D. 2019. On being a graduate student of Robert J. Baker: prospects, perils, and philosophies – lessons learned. Pp. 847-860 in From field to laboratory: A memorial volume in honor of Robert J. Baker (R. D. Bradley, H. H. Genoways, D. J. Schmidly, and L. C. Bradley, eds.). Special Publications, Museum of Texas Tech University 71:xi+1-911. 188. Swier, Vicki J., Robert D. Bradley, Frederick F. B. Elder, and Robert J. Baker. 2019. Primitive karyotype for Muroidea: evidence from chromosome paints and fluorescent G- bands. Pp. 629-642 in From field to laboratory: A memorial volume in honor of Robert J. Baker (R. D. Bradley, H. H. Genoways, D. J. Schmidly, and L. C. Bradley, eds.). Special Publications, Museum of Texas Tech University 71:xi+1-911. 187. Keith, Megan S., Roy Neal Platt II, and Robert D. Bradley. 2019. Molecular data indicate that Isthmomys is not aligned with Peromyscus. Pp. 613-628 in From field to laboratory: A memorial volume in honor of Robert J. Baker (R. D. Bradley, H. H. Genoways, D. J. Schmidly, and L. C. Bradley, eds.). Special Publications, Museum of Texas Tech University 71:xi+1-911.