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Dispersal in the Coahuilan Box Turtle

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Dispersal in the Coahuilan Box Turtle 1 Running title: Dispersal in the Coahuilan box turtle In press, Molecular Ecology 2 3 4 CONTRASTING DEMOGRAPHIC AND GENETIC ESTIMATES OF DISPERSAL IN THE 5 6 ENDANGERED COAHUILAN BOX TURTLE: A CONTEMPORARY APPROACH TO 7 8 CONSERVATION 9 10 Jennifer G. Howeth1,4, Suzanne E. McGaugh2, Dean A. Hendrickson1,3 11 12 MEC-08-0399 Final 13 1 Section of Integrative Biology 14 University of Texas at Austin 15 1 University Station C0930 16 Austin, Texas 78712 17 Phone: 512 475 8669 18 Fax: 512 471 3878 19 20 2 Department of Ecology, Evolution, and Organismal Biology 21 Iowa State University 22 251 Bessey Hall 23 Ames, Iowa 50011 24 25 3 Texas Natural Science Center, Texas Natural History Collection 26 University of Texas at Austin 27 PRC 176 / R4000 28 10100 Burnet Road 29 Austin, Texas 78758 30 31 4 Corresponding author: [email protected] 32 Abstract: 249 / 250 words 33 Main text: 7,641 / 8,000 words 34 Figures: 5; Supplementary Figures: 2 35 Tables: 3; Supplementary Tables: 2 36 37 38 Keywords: connectivity, isolation by distance, metapopulation, microsatellite, mark-recapture, 39 habitat fragmentation 40 Abstract 41 42 The evolutionary viability of an endangered species depends upon gene flow among subpopulations 43 and the degree of habitat patch connectivity. Contrasting population connectivity over ecological and 44 evolutionary timescales may provide novel insight into what maintains genetic diversity within 45 threatened species. We employed this integrative approach to evaluating dispersal in the critically 46 endangered Coahuilan box turtle (Terrapene coahuila) that inhabits isolated wetlands in the desert- 47 spring ecosystem of Cuatro Ciénegas, Mexico. Recent wetland habitat loss has altered the spatial 48 distribution and connectivity of habitat patches; and we therefore predicted that T. coahuila would 49 exhibit limited movement relative to estimates of historic gene flow. To evaluate contemporary 50 dispersal patterns, we employed mark-recapture techniques at both local (wetland complex) and 51 regional (inter-complex) spatial scales. Gene flow estimates were obtained by surveying genetic 52 variation at nine microsatellite loci in seven subpopulations located across the species’ geographic 53 range. The mark-recapture results at the local spatial scale reveal frequent movement among wetlands 54 that was unaffected by inter-wetland distance. At the regional spatial scale, dispersal events were 55 relatively less frequent between wetland complexes. The complementary analysis of population 56 genetic substructure indicates strong historic gene flow (global FST = 0.01). However, a relationship of 57 genetic isolation by distance across the geographic range suggests that dispersal limitation exists at the 58 regional scale. Our approach of contrasting direct and indirect estimates of dispersal at multiple spatial 59 scales in T. coahuila conveys a sustainable evolutionary trajectory of the species pending preservation 60 of threatened wetland habitats and a range-wide network of corridors. 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 2 84 Introduction 85 86 The degree of dispersal between habitats and subpopulations can profoundly impact the demographic 87 and evolutionary trajectory of a species (Bohonak 1999; Clobert et al. 2004). Dispersal affects these 88 trajectories by mediating the abundance and exchange of individuals between subpopulations (Tilman 89 et al. 1997; Hanski 1999) and the distribution of alleles across the landscape through gene flow 90 (Hastings & Harrison 1994; Manel et al. 2003; Storfer et al. 2007). As a consequence of the critical 91 role of connectivity in the maintenance of genetic diversity and adaptive potential, understanding 92 patterns of dispersal in endangered species remains a central focus of conservation assessments 93 (Allendorf & Luikard 2007). In empirical studies, dispersal rates are typically evaluated from either an 94 ecological or ‘direct’ approach where movement is tracked across the landscape or an evolutionary or 95 ‘indirect’ approach where dispersal is inferred from genetic data (reviewed in Bohonak 1999). A strict 96 evolutionary approach to evaluating dispersal may detect high gene flow in a threatened species but 97 could fail to acknowledge fragmentation-induced restriction in contemporary movement. Thus, by 98 adopting one approach to evaluating dispersal, only partial information about population genetic 99 structure and the determining mechanism may be elucidated and the results can thereby misinform 100 conservation efforts. 101 102 Evaluating dispersal over ecological and evolutionary timescales can assess both patterns of 103 gene flow and the demographic processes that may maintain them (e.g. Watts et al. 2004; Wilson et al. 104 2004; Boulet et al. 2007). Patterns of gene flow between subpopulations may serve as a fingerprint of 105 connectivity prior to habitat alteration and the consequential disruption of movement (Palsboll et al. 106 2007; Schwartz et al. 2007). In such cases, the combined effects of fragmentation-induced changes in 107 modern movement and effective population sizes may not maintain historic allele frequencies in 108 subsequent generations (Palsboll et al. 2007; Schwartz et al. 2007). In this paper, we suggest that the 109 degree to which direct observations of dispersal correspond to the indirect estimate gives an indication 110 of how well current demographic processes relate to historic connectivity in recently fragmented 111 populations. This complementary assessment of dispersal in endangered species experiencing habitat 112 loss can consequently expose the potential for a human-induced shift in evolutionary trajectory. 113 114 Wetland turtles are among the organisms most threatened by habitat loss and degradation 115 (Parker & Whiteman 1993; Joyal et al. 2001), and thus these taxa may be especially vulnerable to 116 fragmentation-induced decoupling of contemporary demography and historic gene flow. Species 117 inhabiting the natural patch-matrix mosaic of wetland habitats often exhibit metapopulation dynamics 118 (Joyal et al. 2001; Marsh & Trenham 2001), and as wetlands are lost or fragmented, the stepping 119 stones facilitating dispersal are removed (Parker & Whiteman 1993; Bohonak & Jenkins 2003). For 120 such species that are patchily distributed, landscape characteristics including interpatch distance 121 (Marsh et al. 2000) and patch size (Hanski 1994; Hanski 1999) are important in regulating patch 122 dynamics and ultimately spatial genetic structure (Manel et al. 2003; Storfer et al. 2007). In 123 freshwater turtles, population genetic structure is shaped by both local dispersal behavior within a 124 subpopulation (Freedberg et al. 2005) and regional (long-distance) dispersal between subpopulations 125 which determines the extent and frequency of stepping stone movement (Spinks & Shaffer 2005). At 126 the local scale, a single subpopulation may utilize multiple wetland habitat patches that are part of a 127 larger complex of wetlands (Joyal et al. 2001). At the regional scale, stepping stone behavior and 128 barriers to dispersal can regulate the exchange of alleles between subpopulations and may generate 129 patterns of genetic isolation by geographic distance (Spinks & Shaffer 2005). Fragmentation-induced 3 130 regional dispersal limitation in wetland turtles can lead to closed subpopulations that eventually suffer 131 from reduced genetic variation, are vulnerable to inbreeding depression and drift, and consequently 132 may leave individuals with a limited capacity to adapt to changing environments (Templeton et al. 133 1990; Parker & Whiteman 1993; Kuo & Janzen 2004). 134 135 In this study, we contrast patterns of movement and historic gene flow in the critically 136 endangered Coahuilan box turtle, Terrapene coahuila (Emydidae), endemic to the desert-spring 137 ecosystem of Cuatro Ciénegas, Mexico to test for effects of habitat fragmentation on contemporary 138 dispersal. The isolated 84,000 ha Cuatro Ciénegas valley supports over 70 described endemic species 139 (Secretaría del Medio Ambiente y Recursos Naturales 1999) and serves as a focal landscape for 140 conservation in human-altered environments (Abell et al. 2000; Hendrickson et al. in press). The rich 141 biodiversity and fragmented aquatic habitats of Cuatro Ciénegas recently prompted declaration of the 142 region as a UNESCO Biosphere Reserve (UNESCO-MAB 2006). Terrapene coahuila, the only 143 aquatic species of the genus, inhabits both permanent and seasonal wetlands that are widely distributed 144 across the Cuatro Ciénegas valley (Webb et al. 1963; Brown 1974; Van Dijk et al. 2007). These 145 wetland habitats have become substantially fragmented over the last half century due to water 146 extraction and diversion via a complex canal system (Minckley 1992; Abell et al. 2000; Souza et al. 147 2006; Van Dijk et al. 2007; Hendrickson et al. in press). As a consequence, T. coahuila is listed by the 148 World Conservation Union (IUCN) and the United States Fish and Wildlife Service (USFWS) as 149 ‘endangered’ because of the habitat loss and associated restricted geographic range (USFWS 1973; 150 Van Dijk et al. 2007). The geographic distribution of the box turtle has been reduced from an 151 estimated 600 km2 in the 1960’s to approximately 360 km2 in 2002 (Van Dijk et al. 2007). 152 153 Wetland habitat loss has resulted in relatively isolated subpopulations of T. coahuila (Van Dijk 154 et al. 2007), thereby potentially constraining
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