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Inbreeding Depression and Mating System Evolution in the Perennial Herb Viola Septemloba; and the Evolutionary Maintanence of Cleistogamy Christopher G

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Inbreeding Depression and Mating System Evolution in the Perennial Herb Viola Septemloba; and the Evolutionary Maintanence of Cleistogamy Christopher G Florida State University Libraries Electronic Theses, Treatises and Dissertations The Graduate School 2004 Inbreeding Depression and Mating System Evolution in the Perennial Herb Viola Septemloba; and the Evolutionary Maintanence of Cleistogamy Christopher G. Oakley Follow this and additional works at the FSU Digital Library. For more information, please contact [email protected] THE FLORIDA STATE UNIVERSITY COLLEGE OF ARTS AND SCIENCES INBREEDING DEPRESSION AND MATING SYSTEM EVOLUTION IN THE PERENNIAL HERB VIOLA SEPTEMLOBA; AND THE EVOLUTIONARY MAINTANENCE OF CLEISTOGAMY By CHRISTOPHER G. OAKLEY A Thesis submitted to the Department of Biological Science In partial fulfillment of the requirements for the degree of Master of Science Degree Awarded: Fall Semester, 2004 The member of the Committee approve the thesis of Christopher G. Oakley defended on July 12, 2004. Alice A. Winn Professor Directing Thesis David Houle Committee Member Joseph Travis Committee Member Approved: Timothy S. Moerland, Chair, Department of Biological Science The Office of Graduate Studies has verified and approved the above named committee members. ii ACKNOWLEGEMENTS I would like to especially thank Alice Winn, David Houle and Joseph Travis for their help and advice throughout the course of my studies. I would also like to thank Ken Moriuchi, Jean Burns Moriuchi, Karen Jacobsen, and David Low for help with the field and greenhouse experiments, and /or reviewing parts of this work, and a special thanks to the Florida State University presidential research fellowship for funding during a portion of my studies. iii TABLE OF CONTENTS List of Tables ..…………………………………………………………………………v List of Figures ..………………………………………………………………………..vi Abstract ..………………………………………………………………………………vii INTRODUCTION ………………………...…………………………………………….1 1. INBREEDING DEPRESSION AND MATING SYSTEM EVOLUTION IN THE CLEISTOGAMOUS PERENNIAL VIOLA SEPTEMLOBA ………………..…4 2. THE MAINTINANCE OF CLEISTOGAMY AS A MIXED-MATING SYSTEM ………………………………………………………………………………35 CONCLUSION ………………………………………………………………………..51 REFERENCES ……………………………………………………………………….53 BIOGRAPHICAL SKETCH ………………………………………………………….63 iv LIST OF TABLES Table 1.1………………………………………………………………………………..26 Table 1.2………………………………………………………………………………..27 Table 1.3………………………………………………………………………………..28 Table 1.4………………………………………………………………………………..28 Table 1.5………………………………………………………………………………..29 Table 1.6………………………………………………………………………………..29 Table 1.7………………………………………………………………………………..30 Table 2.1………………………………………………………………………………..49 Table 2.2………………………………………………………………………………..50 Table 2.3………………………………………………………………………………..50 v LIST OF FIGURES Figure 1.1……………………………………………………………………………….31 Figure 1.2……………………………………………………………………………….31 Figure 1.3……………………………………………………………………………….32 Figure 1.4……………………………………………………………………………….33 Figure 1.5……………………………………………………………………………….34 vi ABSTRACT The persistence of mixed mating systems in plants, in spite of theory suggesting that either complete outcrossing or selfing should evolve depending on the level of inbreeding depression, has become a classic puzzle in evolutionary biology. Despite the central role of inbreeding depression in the theory for the evolution of mating systems, the majority of published estimates of inbreeding depression are for annual species, are incomplete, or are measured in artificial environments, calling into question their general utility. I measured inbreeding depression in the field and greenhouse, for all life history stages including male and female reproductive fitness, of a perennial cleistogamous species. I found greater inbreeding depression in the greenhouse (33%) than in the field (11%), but in both cases, inbreeding depression was lower than the threshold required by models to promote outcrossing; however there was considerable variation in the magnitude of inbreeding depression expressed among maternal plants. Inbreeding depression alone is unlikely to be sufficient to explain the persistence of mixed mating in this species. Cleistogamy, a system of dimorphic flowering in which individuals produce both open flowers, and closed obligately selfing flowers, is a mixed mating system which appears to be stable. I reviewed mathematical and verbal models of the maintenance of cleistogamy, as well as relevant published empirical data. Mathematical models require an inherent advantage of CH outcrossing, but do not address the mechanism for such an advantage. I found that CL flowers are generally cheaper to produce, have a higher probability of fertilization, and produce progeny that experience relatively low levels of inbreeding depression. Verbal bet-hedging models provide the most general explanation for the maintenance of CH flower production, given the many advantages of CL reproduction. Future theoretical and empirical work should address how temporal vii variation, in selection for genetically variable progeny, or in male outcrossing success may act to stabilize mixed CH/CL. viii INTRODUCTION The mating system of a species or population, particularly the degree to which individuals mate with related vs. non-related individuals plays a key role in evolution, shaping the underlying population structure and patterns of genetic variation (reviewed in Jain 1976). Flowering plants in particular exhibit a tremendous diversity of mating strategies. Many are hermaphroditic and are therefore capable of self-fertilization, the most extreme form of mating with relatives. Hermaphroditic flowering plants have evolved many elaborate mechanisms to promote cross-fertilization, the benefits of which are believed to include increased genetic variability and consequently, the ability to adapt to new environments. Another genetic benefit of outcrossing is the avoidance of inbreeding depression, the reduction in fitness of selfed relative to outcrossed progeny (Darwin 1876, Charlesworth and Charlesworth 1987). There are however, many potential advantages to self-fertilization (reviewed in Jain 1976). Selfing may provide reproductive assurance, guaranteeing the ability to reproduce even when conditions for outcrossing are unfavorable (Darwin 1876). A selfing individual, that can still donate pollen for outcrossing, also has the advantage of transmitting more copies of its genes to the next generation than an obligate outcrosser (Fisher 1941, Nagylaki 1976). Habitually selfing species may also preserve beneficial gene combinations (Mather 1973), and may be able purge their genetic load of deleterious recessive alleles (Lloyd 1979, Lande and Schemske 1985, Charlesworth and Charlesworth 1987). Given these numerous advantages to selfing, it is not surprising that we observe a variety of mechanisms by which plants promote self-fertilization. 1 Over the course of evolutionary history, selfing species are thought to have arisen from outcrossing progenitors (reviewed in Jain 1976), and the continued evolution of the selfing rate in populations, the juxtaposition of the benefits of selfing against the negative effects of inbreeding depression, has become a classic puzzle in evolutionary biology. Basic theory suggests that in most cases, mixed selfing and outcrossing should not be evolutionarily stable, and that either complete selfing or complete outcrossing should evolve depending on the level of inbreeding depression (Maynard Smith 1978, Lloyd 1979, Feldman and Christiansen 1984, Lande and Schemske 1985, Charlesworth et al. 1990). The abundance of species with intermediate selfing rates remains largely a mystery (Schemske and Lande 1985, Barrett and Eckhardt 1990). Additional theory suggests that under certain conditions, mixed mating could be stable, but the data needed to evaluate the realism of such conditions is scarce (reviewed in Uyenoyama 1993). I present estimates of inbreeding depression for all life history stages, including male and female reproductive fitness, of a perennial plant species with a mixed mating system. Measures of inbreeding depression in the literature are numerous, but many are incomplete and/or were made in an artificial environment, and studies of perennials are not well represented. Previous empirical and theoretical work suggests that estimates of inbreeding depression may be greatly influenced by life history, and the environment in which it is measured (Husband and Schemske 1996, Morgan et al. 1997). If we are to begin to understand mating system evolution in nature, complete and accurate measures of inbreeding depression are a critical first step. I also present a review of studies on the evolutionary maintenance of cleistogamy. Cleistogamy, a system of dimorphic flowering in which individuals produce both open, potentially outcrossed, as well as closed, obligately selfing flowers, is probably the most clear-cut case of facilitated mixed-mating (Lord 1981). It is an interesting syndrome because the closed flowers are generally much cheaper to produce, giving yet another advantage to selfing, and making the persistence of outcrossing all the more puzzling. I review mathematical and 2 verbal models of the maintenance of mixed flower production, many of which weigh the costs of reproduction of each flower type against the relative fitness of progeny (as influenced by, for example, inbreeding depression of the selfed progeny) produced from each flower type. I summarize existing empirical data on relative costs and fitness benefits, and point out potential areas where our knowledge is deficient. I also suggest additional data that are needed, and what new approaches could advance our understanding of how this balance of
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