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IN the SOUTHERN ROCKY MOUNTAINS By EVOLUTION & CONSERVATION OF CUTTHROAT TROUT (ONCORHYNCHUS CLARKII SSP.) IN THE SOUTHERN ROCKY MOUNTAINS by SIERRA MAGENTA LOVE STOWELL B.A., University of Colorado 2007 A thesis submitted Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Master of Arts Department of Ecology and Evolutionary Biology 2011 This thesis entitled Evolution & Conservation of Cutthroat Trout (Oncorhynchus clarkii spp.) in the Southern Rocky Mountains written by Sierra Magenta Love Stowell has been approved for the Department of Ecology & Evolutionary Biology Andrew Martin Sharon Collinge Christy McCain Date The final copy of this thesis has been examined by the signatories, and we find that both the content and the form meet acceptable presentation standards of scholarly work in the above mentioned discipline. Love Stowell, Sierra Magenta (M.A., Ecology & Evolutionary Biology) Evolution & Conservation of Cutthroat Trout (Oncorhynchus clarkii ssp.) in the Southern Rocky Mountains Thesis directed by Dr. Andrew P. Martin ABSTRACT Cutthroat trout are endemic to the cold waters of the American West. The subspecies probably evolved in isolated drainages during the Quaternary. I developed nuclear DNA markers to distinguish between closely related subspecies and estimate divergence times between populations in the southern Rocky Mountains. The subspecies native to Colorado are much older than previous estimates: using a molecular clock, I estimated that greenback and Colorado River cutthroat trout split 0.79 MYA. Human movement of fish has obscured the evolutionary legacy of cutthroats. I used assessments of purity and stocking records for Rocky Mountain National Park, combined with Geographic Information Systems, to assess the utility of geographic measures to serve as proxies for propagule pressure. I found no significant relationships among genetic purity, geographic configuration of roads and trails, and stocking history. Understanding the evolutionary history and the role of human actions in altering evolutionary history has important implications for conservation. iii ACKNOWLEDGMENTS This research was made possible with funding from the Department of Ecology & Evolutionary Biology of the University of Colorado, the Colorado Division of Wildlife, the United States Fish & Wildlife Service, and the National Park Service. Jessica Metcalf provided invaluable advice and a wealth of knowledge on the conservation genetics of cutthroat trout. Chris Kennedy provided information on stocking records of fish in Colorado. Joshua Lamm steadfastly supported teaching, research, and writing efforts. iv CONTENTS CHAPTER 1: INTRODUCTION ……………………………………………………………... 1 CHAPTER 2: HISTORICAL BIOGEOGRAPHY OF CUTTHROAT TROUT IN THE SOUTHERN ROCKY MOUNTAINS ………………………………………………... 5 Introduction …………………………………………………………………………….. 5 Materials and Methods ……………………………………………………………….. 11 DNA Sampling & Amplification………………………………………………… 12 Phylogenetic Analysis ………………………………………………………….. 17 Results …………………………………………………………………………………. 19 Nuclear DNA …………………………………………………………………… 19 Combined Phylogenetic Analysis ………………………………………………. 21 Estimates of Divergence ……………………………………………………….. 24 Discussion ……………………………………………………………………………... 26 Young or Old? ...................................…………………………………………... 26 Over and Over or Over and Around?………………………………………....... 27 Conclusions ……………………………………………………………………………. 29 CHAPTER 3: PREDICTING THE GENETIC PURITY OF CUTTHROAT TROUT IN A HEAVILY STOCKED NATIONAL PARK ………………………………………... 30 Introduction …………………………………………………………………………… 30 Materials and Methods ……………………………………………………………….. 37 Genetic Sampling & DNA Analysis ……………………………………………. 37 Morphological Assessments of Purity & Stocking Data Base………………….. 38 Geographic Information System ……………………………………………….. 39 Statistical Analyses …………………………………………………………….. 40 Results …………………………………………………………………………………. 41 Molecular Genetic Purity ……………………………………………………… 41 Purity and Anthropogenic Features …………………………………………… 43 Anthropogenic Features and Stocking Records ……………………………….. 47 Purity and Stocking Records …………………………………………………... 49 Discussion ……………………………………………………………………………... 51 Conclusions …………………………………………………………………………… 54 CHAPTER 4: CONCLUSIONS ……………………………………………………………... 55 SOURCES ………..……………………………………………………………………………. 58 APPENDIX: POPULATIONS & SPATIAL DATA ………………………………………... 67 v LIST OF TABLES Table 2.1- Final primer details for nuclear loci ………………………………………………... 13 Table 2.2- Details of populations used in phylogenetic analysis ……………………………… 15 Table 2.3- Descriptive statistics for nuclear and mitochondrial sequence data ……………….. 20 Table 3.1- Populations used in molecular genetic analysis of purity …………………………. 41 Table 3.2- Generalized linear model regression results for all data …………………………… 44 Table 3.3- Linear regression models for propagule pressure and spatial descriptions ………... 47 Table 3.4- Generalized linear models for purity and stocking ………………………………… 50 vi LIST OF FIGURES Figure 2.1- Historical ranges of the extant subspecies of cutthroat trout ………………………. 6 Figure 2.2- Behnke’s hypothesis of diversification …………………………………………….. 8 Figure 2.3- Metcalf’s hypothesis of diversification …………………………………………….. 9 Figure 2.4- Map of cutthroat trout populations targeted for analyses …………………………. 16 Figure 2.5- Bayesian phylogenetic tree of nuclear loci ……………………………………….. 21 Figure 2.6- Bayesian phylogenetic tree of ND2 ………………………………………………. 22 Figure 2.7- Bayesian phylogenetic tree of nuclear and mitochondrial loci …………………… 23 Figure 2.8- Phylogenetic estimation of divergence …………………………………………… 25 Figure 3.1- Stocking intensity in Rocky Mountain National Park ……………………………. 33 Figure 3.2- Genetic purity of cutthroat trout in RMNP ……………………………………….. 34 Figure 3.3- Roads and trails in RMNP ………………………………………………………… 35 Figure 3.4- Purity and distance to features by grade ………………………………………….. 45 Figure 3.5- Purity and density of features by haplotype ………………………………………. 45 Figure 3.6- Generalized linear models for purity and features by haplotype …………………. 46 Figure 3.7- Linear models for propagule pressure and features ……………………………… 48 vii CHAPTER 1 INTRODUCTION: CONSERVATION GENETICS OF CUTTHROAT TROUT The greenback cutthroat trout (Oncorhynchus clarkii stomias) is among the most colorful of the cutthroat trout subspecies. The gular folds are characteristically light to deep red, reflecting the species’ common name, while the brownish-olivaceous back is dotted with large black spots and the paler belly ranges from light yellow to melon orange (Young 2009). This beautiful trout was described and named by E. D. Cope in 1872 (Behnke 1992). Native to the South Platte and Arkansas drainages on the eastern slope of the Continental Divide in Colorado, the greenback occupied cold water streams, rivers and lakes above 3,000 m down to the plains, feeding omnivorously on invertebrate matter (Coleman 2007). With the arrival of European- Americans in Colorado in the mid-19th century, the greenback spiraled toward extinction under the combined pressures of over-exploitation for recreation and subsistence; habitat degradation from mining, agriculture, and hydrological alterations; and displacement by and hybridization with introduced species. By 1919, the greenback was absent from the South Platte and was rarely caught by anglers in the upper reaches of the Arkansas (Wiltzius 1985). By 1937 the greenback was declared extinct (Green 1937). In 1953, a graduate student on a camping trip in the mountains above Boulder, Colorado caught a trout he did not recognize. Experts soon verified that the greenback had been rediscovered and a search was enacted to find more remnant populations of greenbacks across their former range. Multivariate morphological analysis of meristic markers, coupled with professional intuition, provided evidence for at least nine populations of supposedly pure greenbacks, including the stream in which the original trout was caught. The rediscovered greenback cutthroat trout was afforded federal protection under the Endangered Species Act (1973). A massive restoration effort was launched in 1978. Introduced and hybridized populations were eradicated from native habitat using electroshock fishing or chemical treatment with rotenone or antimycin and pure greenbacks from the remnant populations were stocked into the cleared habitat (USFWS 1998; Young 2009). Brood stock from remnant populations were cultivated in hatcheries and released into more than 30 restored waters, many of those in Rocky Mountain National Park (USFWS 1998). The recovery objective of the restoration plan was delisting of the greenback by the year 2000. Recovery was defined as the documentation of 20 stable populations representing a minimum of 50 hectares of lakes and ponds and 50 kilometers of stream habitat within the native range (USFWS 1983; see Young & Harig 2001). By 1998, managers considered the recovery effort a success and the de-listing of the greenback was considered imminent: over 639,000 individual fish had been distributed between 1985 and 1996 as part of the recovery effort (Young et al. 2002) and twenty stable populations existed, mostly in the South Platte drainage (USFWS 1998). Even though funding had been diminished in 1986, all that remained to be accomplished according to the 1998 Recovery Plan was to establish two additional stable populations in the Arkansas River drainage and to prepare a long-term management plan to cover the greenback following delisting (USFWS 1998). As the greenback
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