Origin and evolution of the unique Australo-Papuan mangrove- restricted avifauna: novel insights form molecular phylogenetic and comparative phylogeographic analyses By Árpád S. Nyári Submitted to the graduate degree program in Ecology and Evolutionary Biology and the Graduate Faculty of the University of Kansas in partial fulfillment of the requirements for the degree of Doctor of Philosophy. ________________________________ Chairperson: A. Townsend Peterson ________________________________ Robert G. Moyle ________________________________ Rafe M. Brown ________________________________ Mark B. Robbins ________________________________ Xingong Li Date Defended: 22 April 2011 The Thesis Committee for Árpád S. Nyári certifies that this is the approved version of the following thesis: Origin and evolution of the unique Australo-Papuan mangrove-restricted avifauna: novel insights form molecular phylogenetic and comparative phylogeographic analyses. ________________________________ Chairperson A. Townsend Peterson Date approved: 22 April 2011 II Abstract Coastal mangrove forests of Australo-Papua harbor the world’s richest avifauna restricted to mangroves, however their biogeographic origins and evolutionary processes shaping their current distributions are not well understood. Building upon previous work based on field surveys and morphological characters, I am here focusing on elucidating the phylogenetic placement of mangrove-bound species from three different bird families as well as the comparative phylogeographic analysis of eight co- distributed mangrove restricted birds. In the first molecular phylogenetic analysis of fantails (Aves: Rhipiduride) I document six distinct clades, harboring members spread across large geographic extents. Rhipidura hypoxantha is not a true fantail, but rather a member of the Stenostiridae clade that is morphologically and behaviorally convergent with fantails. The Australian mangrove fantails R. phasiana and R. dryas both evolved recently from Pacific island radiations. A molecular phylogeny of all extant species of the honeyeater genus Lichenostomus (Aves: Meliphagidae) also addresses the relationship of the only mangrove-restricted honeyeaters on Australia’s east coast, L. versicolor and L. fasciogularis. These species were not sisters but rather L. versicolor was sister to the pair comprising L. fasciogularis and the continental widespread Singing Honeyeater L. virescens. The genus Lichenostomus is not monophyletic, and instead comprises seven distinct lineages interdispersed within the larger meliphagid assemblage. Based on this III taxonomic and nomenclatural revision, recognition of a novel genus of honeyeater is warranted. A multilocus molecular phylogeny of gerygones (Aves; Acanthizidae) establishes that the three mangrove endemic species do not form a monophyletic clade, instead indicating three distinct, temporally non-overlapping, radiations into magroves. Moreover, G. cinerea from New Guinea is in fact a member of the genus Acanthiza, with which it consistently grouped based on 13 distinct molecular loci analyzed. Comparative phylogeographic analyses of 8 co-distributed mangrove forest endemic birds concludes biogeographic barriers such as the Canning Gap, Bonaparte Gap, and the Carpentarian Gaps all had important, but varying degrees of impact on the species we analyzed. Species with more recent radiations into mangroves include Rhipidura phasiana, Myiagra ruficollis, and Myzomela erythrocephala, while Peneoenanthe pulverulenta, Pachycephala melanura, P. lanioides, Zosterops luteus, and Colluricincla megarhyncha all had more marked phylogeographic signatures. IV Acknowledgements I would like to thank first and foremost my academic advisor, A. Townsend Peterson for his generous and kind support throughout my time as a graduate student. Even though I was coming from a country where speciment-based ornithological studies have fallen significantly behind European, yet alone global standards, Town accepted me at his side and made possible an amazing suite of opportunities that allowed me to learn and appreciate the challenges, coordination, and rewards of modern collections- based research. My fellow committee members Rob Moyle, Rafe Brown, Mark Robbins and Xingong Li have lent their valuable time and expertise for the duration of my stay at KU, for which I am deeply endebted. Mark Robbins was instrumental also in shaping and broadening my training as a field ornithologist. Thanks to his life-long experience, passion and contagious energy, I can now say that I have become an integral part of the community whose aim is to promote the practices and ideals of current natural history museum collections and specimen-based research. In short, I will never forget those amazing expeditions made possible by the wonderful people at the Division of Ornithology and the KU Natural History Museum. The foundations of the present research have been layed by extesive field work conducted by active and passionate people, among which Julian Ford, Ian Mason, Richard Schodde, and Leo Joseph have played seminal roles. Julian, Ian and Richard collected and summarized many of their findings on Australia’s amazing mangrove birds, providing a rich testing ground for the work herein. Leo has of course been the person who graciously allowed me to utilize the tremendous resources at the Australian National Wildlife Collection, and also made possible an important collecting expedition V into the mangroves of the Northern Territory. My childhood obsession with the Australian continent has thus been nurtured further by the expertise and helpfulness of many people I met there: Deryn Alpers, Ken Aplin, Walter Boles, Mark Burrows, Mark Clayton, Alex Drew, Denise Hardesty, Ron Johnstone, Suzanne Metcalfe, Robert Palmer, and Lynn Pedler. Support for this work in the form of specimen loans was made possible by many museum collections: American Museum of Natural History (J. Cracraft and P. Sweet), Field Museum of Natural History (J. Bates, S. Hackett, and D. Willard), Louisiana State University Museum of Natural Science (R. Brumfield and D. Dittmann), Massey Umiversity (S. Trewick), National Museum of Natural History, Smithsonian Institution (G. Graves and J. Dean), Western Australian Museum (R. Johnstone and C. Stevenson), and Zoological Museum University of Copenhagen (J. Fjeldså). Funding was provided by CSIRO Ecosystems Science (CES), the Atlas of Living Australia, University of Kansas Biodiversity Institute, Leaman Harris Fund, the American Museum of Natural History Frank M. Chapman Memorial Fund, and the American Philosophical Society. Since field work and expeditions have played a major role in my graduate student time at KU, I would like to thank many amazing people for their support, expertise, and companionship: Nate Rice, Oliver Komar, Guojun Chen, Roger Boyd, Dale Clayton, Sarah Bush, Burton Lim, Judith Eger, Enrique Arbelaez-Cortes, and Walter Wehtje, all of whom have taught me a lot. The KU Biodiversity Institute and the KU Department of Ecology and Evolutionary Biology have played an essential supportive role through continuous promotion of sources of funding, ideas and collaborations. Extraordinary faculty members and research associates whose teachings and advice I am grateful for VI include Christopher Filardi, Mark Holder, John Kelly, Andrew Mack, Adolfo G. Navarro- Sigüenza, Richard Prum, John Simmons, Jorge Soberón, Robert Timm, Linda Trueb, and Edward O. Wiley. Fellow graduate students and friends have played an equally important role, providing invaluable sources of ideas, moral support, and good times, which I will dearly miss and never forget. Francine Abe, Adorian Ardelean, Marina Anciaes, Michael Andersen, Narayani Barve, Brett Benz, Elisa Bonaccorso, Andrea Crowther, Elena Brebenel, Matt Davis, Shannon DeVaney, Jake Esselstyn, Mike Grose, Juan Manuel Guayasamin, Ismael Hinojosa, Liza Holeski, Pete Hosner, Alberto Jimenez-Valverde, Charles Linkem, Andres Lira Noriega, Seah Maher, Enrique Martinez, Yoshinori Nakazawa, Jaime Oaks, Carl Oliveros, Luis Antonio Sanchez, Eric Settles, Cameron Siler, Jeet Sukumaran, Corey Welch and Richard Williams. Fond memories go back to the time spent with Alexis F.L.A. Powell discussing biology, optics, birding and life in general. Karen Willey and Scott Eudaly have always been ready to lend a helping hand. Several other people were instrumental in providing help with logistics, paperwork, and overall daily student life. Leonard Krishtalka, Jordan Yochim and Lori Schlenker at the KUNHM, Jaime Keeler at KUEEB, and Lynne Vanahill at the KUISSS are here especially acknowledged. My heart goes out to my family back home in Romania, who has seen me leave their caring side in order to pursue my own dreams. Words cannot describe de gratitude and respect I have for them and the sacrifices they made for me. I am especially saddened that my grandparents did not live to see me get to this stage in life, however I hope that their ideals continue to live on throughout my work and my remaining lifetime. VII My wonderful and kind wife Mona was always on my side and in my heart, providing a comforting and loving feeling during difficult times. During Mona’s postdoc in Madison, we have met some old and new friends, who I would like to acknowledge for their wonderful warm company during those cold Wisconsin months. VIII Table of contents Abstract iii Acknowledgements v Chapter 1: Phylogenetic relationships of fantails (Aves: Rhipiduridae 11 Introduction 13 Materials and Methods