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Viewed by Rieseberg 1995, Rieseberg and Wendel 1993, Arnold SYSTEMATICS, HYBRIDIZATION, AND CHARACTER EVOLUTION WITHIN THE SOUTHERN AFRICAN GENUS, ZALUZIANSKYA (SCROPHULARIACEAE S.S., TRIBE MANULEEAE) DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Jenny Kay Archibald, B.S. ***** The Ohio State University 2003 Dissertation Committee: Approved by Dr. Andrea D. Wolfe, Adviser Dr. John V. Freudenstein ________________________ Dr. John W. Wenzel Adviser Department of Evolution, Ecology, and Organismal Biology ABSTRACT Zaluzianskya (Scrophulariaceae s.s., tribe Manuleeae), a genus of 55 species of annual and perennial herbs endemic to southern Africa, includes a diverse array of morphological features – particularly in floral morphology. This dissertation examines the genus at both population and species levels. First, a molecular investigation of hybridization between two species in the genus was conducted. Although unexpected due to apparent ethological isolation, hybridization between day-flowering Z. microsiphon and night-flowering Z. natalensis has been proposed based on intermediate individuals found in sympatric populations of these two species. This putative hybridization was studied using molecular markers (ISSRs) and ordination of morphological traits. The species are very genetically similar, but intra- and interspecific variation in band-frequencies was found. Eight of fifteen species-typical ISSR markers occurred at intermediate band frequencies in the putative hybrids compared to the average band frequency for each “parental” species. The other seven markers occurred at extreme frequencies. However, they were not extreme when compared with individual population frequencies of one or both species. At minimum, the hybrid population always had comparable band frequencies to those of one or both sympatric “parental” population(s). These results are consistent with hybridization, although they could also indicate historical similarity. ii Nine loci were present only in individuals of Z. microsiphon, the “hybrids,” and sometimes the sympatric individuals of Z. natalensis (only one locus showed the reverse pattern). This suggests unidirectional gene flow from Z. microsiphon to Z. natalensis, which is also supported by detailed examinations of four marker bands with significant differences in band frequencies across populations. Separate clusters for each species were formed by PCA, with hybrid individuals located between the two clusters but often closer to the Z. natalensis cluster. One hypothesis is that hybrids are backcrossing with Z. natalensis, leading to introgression of Z. microsiphon genetic material. A genus-wide investigation of phylogenetic relationships was also conducted, using DNA sequences of ITS, rpl16, and trnL-trnF to produce the first broad phylogenetic hypotheses for this genus and thus the first tests of the monophyly of the genus and its sections. One of the “outgroups,” Reyemia nemesioides, was derived within Zaluzianskya, with strong support. This is consistent with several morphological characteristics of both species of Reyemia and it is thus proposed that Reyemia be merged into Zaluzianskya. Sections Zaluzianskya and Holomeria are clearly not natural, whereas the status of section Nycterinia is uncertain. The single species sampled from section Macrocalyx was nested within section Nycterinia according to the chloroplast (and combined) data, but sister to that section according to the ITS data. The status of several species was also highlighted by the data. Populations of Z. villosa and Z. gracilis were derived from Z. affinis while Z. divaricata was derived from Z. pusilla. Finally, populations of the sole day-flowering species in section Nycterinia, Z. microsiphon, were separated on the phylogenies. The source of this division is unknown but could possibly be hybridization or convergent evolution via pollinator selection. iii These phylogenetic hypotheses were also used to examine character evolution for eleven traits within Zaluzianskya, focusing on several traits considered important in the classification of the genus as well as floral traits that appear relevant for pollinator interactions. The evolution of habit was also examined along with its potential relation to distribution within different rainfall regimes. The placement of the former species of Reyemia within Zaluzianskya is supported by calyx lobing, and the specific placement of R. nemesioides is supported by stem indumentum and petal shape. The latter two traits generally support the division of Zaluzianskya into three major clades. Nectary adnation supports clade 3 as well as a subclade of clade 1 (Z. affinis + Z. villosa + Z. gracilis) also supported by stamen traits. Long corolla tubes define all of clade 3 except Z. mirabilis and intermediate tubes mark a subclade of clade 1. In contrast, floral symmetry and throat indumentum are largely homoplasious. Several potential implications regarding pollination biology are discussed. First, several floral traits may have evolved in parallel within “Z. microsiphon” lineages due to pollinator selection (long-proboscid fly vs. the hawkmoth pollinators of other members of section Nycterinia), but this is unclear due to the uncertain status of this species. Several other traits found within clade 3, such as a ringlet of hairs around the throat and notched petals, may be beneficial for moth pollination. However, these traits also occur in some other clades and the function in those species, if there is any, is unknown. Reconstructions of the distribution of species of Zaluzianskya within relatively arid vs. mesic regions appear similar to those of habit (annual vs. perennial). The plesiomorphic condition for this group is annual, distributed within arid regions. Subsequent migrations to mesic regions and derivations of the perennial habit both occur only within clade 3. iv Dedicated to Mark and my parents v ACKNOWLEDGMENTS I would like to thank my advisor, Andrea Wolfe, and my committee members, John Freudenstein and John Wenzel, for supporting me in my graduate work. I’d also like to thank Tom Waite for serving on my Candidacy Examination Committee as well as for his assistance with statistical analyses. I thank Mark Mort for his constant encouragement, enthusiasm, generosity, and willingness to argue the minutiae of systematics with me. I am indebted to many current and previous members of the systematics and ecology groups at O.S.U. for assistance with laboratory matters, analyses, editing, and for helpful and interesting discussions. In particular I would like to thank Chris Randle, for his help in all scientific arenas as well as his entertaining discourse; Shannon Datwyler for guidance, especially when I was new to the lab; Theresa Culley and Lisa Wallace, particularly for their insight into population biology; Sibyl Bucheli, Jeff Morawetz, and Sarena Selbo for their encouragement; as well as Nidia Arguedas, Siri Ibarguen, Shawn Krosnick, Paul Nunley, and Kristen Uthus for making O.S.U. a better place both scientifically and generally. Shannon, Andrea, Sarena, Shawn, Mark, and Sibyl are also due thanks for playing the arduous role of dog- and/or plant-sitters during my field work in Africa. I’d also like to thank Erich Grotewold and Allison Snow for allowing me to do vi research with their lab groups. From the University of Kansas, I’d like to thank Dan Crawford and Craig Freeman for helpful discussion and Kristopher Fairfield for assistance in the lab. My work in South Africa was greatly aided by a number of researchers, including Nigel Barker, Nicola Berg, Jo Beyers, Trevor Edwards, Craig Peter, Koos Roux, Frank Smith, Dee Snijman, Kim Steiner, and Tony Verboom, among others. In particular, this work would not have been possible without the assistance and knowledge of Steve Johnson with whom I collaborated for the hybridization studies. Multiple herbaria were also indispensable for my work, including NBG, BOL, GRA, and NU. These institutions were very generous with access to their specimens, resources, and staff. Finally I wish to thank Paul Wolf and Bradley Kropp for giving me my start in scientific research; Audrey Seamons and David Marsolais for their friendship; and my family, for being the way that they are. My work was made possible by funding from an ASPT Graduate Student Research Award, a Molecular Life Science Graduate Fellowship, an Alumni Grant for Graduate Research and Scholarship, Janice Carson Beatley Herbarium Awards, and Graduate Student International Dissertation Research Travel Grants to myself, as well as grants from the National Science Foundation to my advisor (DEB 9708332 and DEB 0089640). vii VITA 6 October 1974 …………………… Born – Logan, UT, USA 1997 ………………………………. B.S. Biology, Utah State University 1997 – 1998 ………………………. Researcher, Utah State University 1998 – present …………………….. Graduate Fellow and Teaching Associate, The Ohio State University PUBLICATIONS Archibald, J. K., M. E. Mort, D. J. Crawford. 2003. Bayesian inference of phylogeny: a non-technical primer. Taxon 52: 187-192. Wolf, P. G., D. R. Campbell, N. M. Waser, S. D. Sipes, T. R. Toler, and J. K. Archibald. 2001. Tests of pre- and postpollination barriers to hybridization between sympatric species of Ipomopsis (Polemoniaceae). American Journal of Botany 88: 213-219. Archibald, J. K., P. G. Wolf, V. J. Tepedino, and J. B. Bair. 2001. Genetic relationships and population structure of the endangered steamboat buckwheat, Eriogonum ovalifolium var.
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