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University of Nevada, Reno Multi-empirical investigations on the population genetic structure, ecological niche, and regeneration of Ivesia webberi with conservation implications A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Ecology, Evolution and Conservation Biology by Israel Temitope Borokini Dr. Mary M. Peacock – Advisor Dr. Peter J. Weisberg – Co-advisor May, 2021 Copyright by Israel Temitope Borokini, 2021 All Rights Reserved THE GRADUATE• SCHOOL We recommend that the dissertation prepared under our supervision by entitled be accepted in partial fulfillment of the requirements for the degree of Advisor Co-advisor Committee Member Committee Member Graduate School Representative David W. Zeh, Ph.D., Dean Graduate School i ABSTRACT Ecosystems often contain a few cosmopolitan species and a large number of rare species. Despite their relative low abundance and biomass, rare species support the multifunctionality and resilience of ecosystems. Therefore, empirical studies on rare and range-restricted species can increase our understanding of eco-evolutionary underpinnings of species and ecosystem persistence, and generate sufficient knowledge to design effective conservation programs. These research studies can also benefit conservation programs for rare and range-restricted species, which are often prioritized. This research focuses on Ivesia webberi, a federally threatened perennial forb and the vegetative communities that harbor the species. Specifically, empirical studies investigated the following: (1) species-environment relationship of I. webberi using iterative and multi-year ecological niche modeling with complementary model-guided sampling, to describe and predict suitable habitats; (2) the relationship between soil seed bank and aboveground vegetation in plant communities where I. webberi is found, to understand the regeneration niche of I. webberi and assess ecological resilience of the vegetative communities; (3) genetic diversity, structure, and functional connectivity among I. webberi populations in order to characterize genetic resources and therefore evolutionary potential; (4) the relationships between genome size variation and bioclimatic variables within I. webberi and among Ivesia taxa; and (5) seed viability of I. webberi, including spatiotemporal variability and storage behavior. Findings from the 5-year iterative niche modeling study resulted in the discovery of seven novel populations, an expansion of the known species distribution range, and identification of important environmental drivers of the ecological niche of I. webberi. ii Native species richness was higher in aboveground vegetation in the sampled sites where I. webberi occurs while the soil seed bank is dominated by invasive annual grasses. This resulted in low floristic similarity between the aboveground vegetation and the soil seed bank, and highlights the importance of seeding with native plants and control of invasive plant species to maintain the ecological legacies of these sites in the Great Basin Desert. Genetic diversity is relatively low across I. webberi populations and exhibited significant spatial genetic structure; functional connectivity was influenced by synergistic effects of geographic distance and landscape features. However, I. webberi exhibits a significant temporal, not geographical, variation in seed viability, and seed viability potentially reduces with storage time suggesting a recalcitrant behavior. Seed viability can be reliably estimated and monitored using non-destructive x-ray imagery and multispectral imaging techniques. An 8-fold variation in genome size of 31 Ivesia taxa was observed, ranging from 0.73 pg/2C in I. baileyi var. beneolens to 5.91 pg/2C in I. lycopodioides ssp. megalopetala. This genome size variation significantly correlated with actual evapotranspiration and seed size. Inference from genome size suggest that all sampled Ivesia are diploid with 28 chromosomes. Similar significant correlations between intraspecific genome size variation in I. webberi and evapotranspiration and seed size were observed; genome size was larger in I. webberi populations closer to the species’ range center and smaller towards the margin. Relatively small genome sizes and their correlations with functional trait and energy availability indicate that genome size has adaptive significance for these desert-adapted species. Overall, the findings of these studies have advanced scientific knowledge on the eco-evolutionary processes in a range- iii restricted plant species in the Great Basin Desert, and provide useful information to design effective conservation programs. iv ACKNOWLEDGEMENTS This dissertation is dedicated to my parents, Pastor Ayodele Borokini and Dr. (Mrs.) Olufunke Borokini, who are constantly on their knees praying for my career success and for their unflinching support and encouragement. I am grateful for the immense support from my wife, Sylvia Borokini, and my daughter, Victoria. I count myself very fortunate to have Dr. Mary Peacock and Dr. Peter Weisberg as my advisors. Their experience, expertise, mentoring, and guidance is unparalleled. I am also grateful to the rest of my academic committee – Dr. Elizabeth Leger, Dr. Ana de Bettencourt Dias, and Dr. Thomas Parchman for their contribution and encouragement throughout the journey. My work has benefited immensely from the support and advice of alumni and faculty in the University of Nevada, Reno (UNR) community - Dr. Julie Allen, Dr. Kevin Shoemaker, Dr. Ken Nussear, Dr. Scott Bassett, Dr. Kelly Klingler, Dr. Sarah Barga, Dr. Phillip Street, Dr. Jane Dell, Dr. Frank Amankonah, Dr. Jacob Francis, Dr. Alfred Schissler, and Mr. Tom Dilts. I am also grateful to my peers in the Ecology, Evolution and Conservation Biology program including Joshua Hallas, Adriana Parra, James Simmons, and Anjana Parandhaman, as well as Charles Edwards of the UNR Social Psychology graduate program, and Gary Sterle of the Hydrology graduate program. I cannot forget other scholars beyond the University who have contributed to data analysis aspects of my research, including Dr. Pierre Legendre, Dr. Town Peterson, Dr. William Peterman, Dr. Javan Bauder, Dr. Scott Buchanan, Dr. Andrew Shirk, Dr. James Birchler, Dr. Georges Damien, and Dr. Samuel Cushman. v I am also grateful to several local botanists, citizen scientists, and conservation managers who contributed to my field surveys, collections, collection permits, and other expert advice. This include, but not limited to Kathryn Birgy (UNLV Herbarium), Elizabeth Scott (Portland State University), Tianxiao Hao (University of Melbourne, Australia), Charlene Duncan, and Arnold Tiehm (UNR), Sarah Kulpa (U.S. Fish and Wildlife Service, Reno Field Office), Valda Lockie (Bureau of Land Management, Susanville CA Office), Janel Johnson and Dr. James Morefield (Nevada Natural Heritage Program), Prof. Tina Ayers (Northern Arizona University), Dr. Duncan Bell and Dr. Naomi Fraga (Rancho Santa Ana Botanical Garden), Dr. Jennifer Wilkening (USFWS Southern Nevada office), Dr. Jeanette Perry and Dr. Patricia Hardesty (Nevada National Security Site), John Christopherson, Gary Reese, and Cayenne Engel (Nevada Department of Forestry), Jordan Brown (Oregon Native Plant Conservation Program, and Department of Botany, Oregon State University), Lindsey Wise (Oregon Biodiversity Information Center), Michael Hagebusch, John Dittes, Dr. Margaret Widdowson, Derek Antonelli, Greg Gust, Tara de Queiroz, and Maura Olivos. The dissertation research was funded through a grant from the U.S. Fish and Wildlife Service, with additional support from the following research grants – UNR EECB summer stipends, UNR Biology Department, California Native Plant Society (CNPS) San Diego chapter mini-grant, CNPS Stebbins fund, Native Plant Society of Oregon field research grant, Utah Native Plant Society grant-in-aid program, CNPS Shasta chapter Oak tree grant, Arizona Native Plant Society Doug Green research grant, and Idaho Native Plant Society education, research and inventory grant, Northern California Botanists (NCB) Botany research scholarship program, the Nevada Native vi Plant Society Margaret Williams research grant, and the Society for Conservation Biology (SCB) graduate student research fellowship. vii TABLE OF CONTENTS Abstract ………………………………………………………………………………… i Acknowledgements ……………………………………………………………………. iv Table of contents ……………………………………………………………………… vii List of Tables ……………………………………………………………………………xi List of Figures ………………………………………………………………………....xiii INTRODUCTION……………………………………………………………………….1 CHAPTER 1 Geographic predictions of iterative ecological niche modeling result in the discovery of novel populations of a rare cold desert perennial …..…….…..31 Abstract …………………………………………………………………….…...32 Introduction ……………………………………………………………….……34 Methods ………………………………………………………………….….…..37 Results …………………………………………………………………………..48 Discussion ………………………………………………………………………52 References ………………………………………………………………….…...61 Tables ……………………………………………………………………….…..77 Figure legends …………………………….……………………………….…....84 Figures …………………………………………………………………………..86 Acknowledgements ………………………………………………………….....95 Supplemental Information ……………………………………………...……..96 CHAPTER 2 Quantifying the relationship between soil seed bank and plant community assemblage in sites harboring the threatened Ivesia webberi in the western Great Basin Desert ……………………………………………………….…...121 viii Abstract ………………………………………………………………………..122 Introduction ………………………………………………………………...…124
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