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The Evolution of Freeze Tolerance in a Historically Tropical Snail Alice B

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The Evolution of Freeze Tolerance in a Historically Tropical Snail Alice B Louisiana State University LSU Digital Commons LSU Doctoral Dissertations Graduate School 2010 The evolution of freeze tolerance in a historically tropical snail Alice B. Dennis Louisiana State University and Agricultural and Mechanical College Follow this and additional works at: https://digitalcommons.lsu.edu/gradschool_dissertations Recommended Citation Dennis, Alice B., "The ve olution of freeze tolerance in a historically tropical snail" (2010). LSU Doctoral Dissertations. 1003. https://digitalcommons.lsu.edu/gradschool_dissertations/1003 This Dissertation is brought to you for free and open access by the Graduate School at LSU Digital Commons. It has been accepted for inclusion in LSU Doctoral Dissertations by an authorized graduate school editor of LSU Digital Commons. For more information, please [email protected]. THE EVOLUTION OF FREEZE TOLERANCE IN A HISTORICALLY TROPICAL SNAIL A Dissertation Submitted to the Graduate Faculty of the Louisiana State University and Agricultural and Mechanical College in partial fulfillment of the requirements for the degree of Doctor of Philosophy in The Department of Biological Sciences by Alice B. Dennis B.S., University of California, Davis 2003 May, 2010 ACKNOWLEDGEMENTS There are many people who have helped make this dissertation possible. I would first like to thank my advisor, Michael E. Hellberg, for his support and guidance. Comments and discussion with my committee: Drs. Sibel Bargu Ates, Robb T. Brumfield, Kenneth M. Brown, and William B. Stickle, have been very helpful throughout the development of this project. I would also like to thank those whose guidance helped lead me down this path, particularly Rick Grosberg, John P. Wares and Alex C. C. Wilson. Physiological trials in 2008 were conducted in the lab of Stephen Loomis at Connecticut College, and could not have been completed without his assistance and contribution to this work. I am grateful to all of those who have helped me with analyses and provided laboratory assistance, especially Patricia C. Arbour-Reily, Peter Beerli, Bryan Carstens, Brent Christner, Ron Eytan, Fernando Galvez, Alice Hudder, Michael Kaller, Joe Neigel, Mohamed Noor, Jen Roach, Jackie Stephens, Deb Triant and Andrew Whitehead. Many people have also helped me with field collections, including Tina Bell, Melanie Bishop, Rachel Collin, Chris Dennis, Ron Eytan, Phillip Fenberg, Kari Galvan, David Johnson, Steve Loomis, Sarafaye Mahon, Ryan Moody, Carlos Prada and Timothy Rawlings. The funding I have received from the National Science Foundation, Louisiana State University Biograds, Louisiana State University Graduate School, AAUW, Sigma Xi, the Conchologists of America and the Society of Wetland Scientists has made much of this work possible. A portion of this research was conducted using the resources of the Cornell Center for Advanced Computing, which receives funding from Cornell University, the National Science Foundation, and other leading public agencies, foundations, and corporations. ii TABLE OF CONTENTS ACKNOWLEDGMENTS…………………………………………………………………….....ii ABSTRACT…………..……………………………………………………………...................iv CHAPTER 1 INTRODUCTION…..……………………………………………………...................1 2 ECOLOGICAL PARTITIONING AMONG PARTIALLY SYMPATRIC CRYPTIC SPECIES …………………………………………………………………………………..….…4 3 TESTING FOR TROPICAL NICHE CONSERVATISM IN A BROADLY DISPERSING MARSH SNAIL (MELAMPUS) …………………………………………………………..….…32 4 IDENTIFICATION OF SEASONALLY UP-REGULATED EXPRESSED SEQUENCE TAGS IN MELAMPUS BIDENTATUS……………………………………………………..……61 5 CONCLUSIONS…………………………………………………………….............76 REFERENCES……………………………………………………………………………..…..79 APPENDIX A: COLLECTION LOCALES FOR ECOLOGICAL NICHE MODELING AND IDENTIFICATION OF CRYPTIC SPECIES……………………………………….......98 APPENDIX B: PRINCIPAL COMPONENT MATRIX…………………………….100 APPENDIX C: SEASONALLY UP-REGULATED TRANSCRIPTS………...……102 VITA…………………………………………………………………………………….…….103 iii ABSTRACT Geographic range differences among species may result from differences in their physiological tolerances. In the intertidal zone, marine and terrestrial environments intersect to create a unique habitat, across which physiological tolerance strongly influences range. The snail Melampus bidentatus occurs in coastal salt marshes in the western Atlantic and Gulf of Mexico. I have used sequence data from one mitochondrial (CO1) and two nuclear markers (histone H3 and a mitochondrial carrier protein, MCP) to identify three cryptic species within Melampus bidentatus, and to infer their relationships to other Melampus. To identify microhabitat differences between two cryptic species, I modeled their distributions using both marine and terrestrial environmental data. Temperature largely explained their range differences, but other environmental components (precipitation, salinity, and tidal height) explained facets of the range that temperature cannot. To test for phylogenetic conservation in freeze tolerance, I tested the mean lower lethal temperature (LT50) of three temperate and three tropical species. Cryptic species of M. bidentatus are significantly more freeze tolerant than their tropical relatives, although there was variation among locales within species, most likely due to microhabitat variation. The temperate species M. floridanus was also freeze tolerant, but without testing the LT50 of its closest relatives in the Pacific, I cannot determine this represents an independent evolution of freeze tolerance, or if this trait is more widely shared among Melampus. Nonetheless, the lack of freeze tolerance in the most basal species that I have tested (M. bullaoides), and the predominantly tropical distributions of most ellobiids, suggests that the evolution of freeze tolerance has allowed for the invasion of the temperate zone by Melampus. Using massively parallel sequencing, I have isolated > 500,000 expressed sequence tags and assembled these into ~20, 000 seasonally expressed transcripts. A comparison of these iv transcripts has revealed 2 candidate markers to test for their association with freeze tolerance in M. bidentatus, and many more markers that can be used for further phylogenetic analyses in Melampus. Further work to examine variation in both the sequence and expression of these proteins is needed to determine if they underlie adaptive differences among species. v CHAPTER 1: INTRODUCTION The causes and consequences of species range limits have been widely studied in evolution and ecology (Gaston, 1998; Gaston, 2000; Gaston, 2003; Gaston, 2009). Across the globe, species occupy ranges that vary widely in both size and in the span of environmental variables they contain. Many groups are cosmopolitan while others species may be restricted to a single mountain, river, or cave (Gaston, 2003). Differences in geographical range are driven by a variety of factors, including environmental tolerance, dispersal, biotic interactions, and history (Engle, Summers, 1999; Sexton et al., 2009). Classically, questions about range were approached through the study of physiology (Spicer, Gaston, 1999), and early ecological studies considered physiological limitations as a central factor limiting the occurrence of a species (Pearce 1939, cited by Spicer, Gaston, 1999). The basis of this observation was that tolerance of local conditions preceded all other forces that would constrain species range. In the time since, this physiological focus was largely replaced by studies of biotic processes, including competition and predation (Connell, 1961; Connell, 1972) and environmental processes such as disturbance and succession (Sousa, 1984). Current research into the determinants of range limits has been greatly expanded, and considers the roles of many factors including dispersal (Leibold et al., 2004; Myers, Harms, 2009), predation (Lee, Silliman, 2006; Silliman, Zieman, 2001) and history (Cunningham et al., 1991; Hickerson, Cunningham, 2005). The physiological basis of range limits has garnered renewed interest for its contribution to latitudinal gradients in species diversity. In particular, the process of tropical niche conservatism hinges on the biological effects of temperature and its limit to geographic range (Castaneda et al., 2004; Harrison, Whitfield, 2006; Stillman, 2002; Wiens, Donoghue, 2004; Wiens, Graham, 2005). Under tropical niche conservatism, peak species richness in the tropics may in part be due to curbs on dispersal from tropical to temperate regions, primarily though 1 limited tolerance of conditions in temperate regions (Gaston, 2009; Wiens, Donoghue, 2004; Wiens, Graham, 2005). Temperature, and freezing conditions in particular, may limit the poleward spread of tropical taxa (Farrell et al., 1992; Hylleberg, Siegismund, 1987; Rivadeneira, Fernandez, 2005; Wiens et al., 2006). If adaptations to deal with cold and freezing temperature arise rarely, their development may restrict tropical species from inhabiting temperate regions. Over time, the limited dispersal from the tropics to temperate regions may contribute to reduced species diversity in temperate regions. This highlights the need for renewed study of the physiological basis of range limits, especially in light of new genetic tools available to look at this in a phylogenetic context. This dissertation sets out to examine the role of physiological differences in shaping species ranges in Melampus, a group of intertidal snails. Melampus occupies coastal salt marshes and mangrove swamps, primarily in tropical regions (Martins, 1996b). Occupying a high intertidal position, Melampus
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