Genetic variation and population structure in a threatened species, the Utah prairie dog Cynomys parvidens: the use of genetic data to inform conservation actions Nathanael L. Brown1, Mary M. Peacock2 & Mark E. Ritchie1 1Department of Biology, Syracuse University, 107 College Place, LSC, Syracuse, New York 13224, Mark Ritchie 2Department of Biology MS314, University of Nevada Reno, 1664 North Virginia Street, Reno 89557, Nevada Keywords Abstract Bayesian genotype clustering analysis, genetic diversity, genetic structure, threatened, Utah The Utah prairie dog (Cynomys parvidens), listed as threatened under the Uni- prairie dog. ted States Endangered Species Act, was the subject of an extensive eradication program throughout its range during the 20th century. Eradication campaigns, Correspondence habitat destruction/fragmentation/conversion, and epizootic outbreaks (e.g., syl- Mary M. Peacock, Department of Biology vatic plague) have reduced prairie dog numbers from an estimated 95,000 indi- MS314, 1664 North Virginia Street, viduals in the 1920s to approximately 14,000 (estimated adult spring count) University of Nevada, Reno, Reno, NV 89557. today. As a result of these anthropogenic actions, the species is now found in Tel: (775) 784-1958; Fax: (775) 784-1302; small isolated sets of subpopulations. We characterized the levels of genetic E-mail: [email protected] diversity and population genetic structure using 10 neutral nuclear microsatel- lite loci for twelve populations (native and transplanted) representative of the Present address three management designated “recovery units,” found in three distinct biogeo- Nathanael L. Brown, Utah Field Office, United graphic regions, sampled across the species’ range. The results indicate (1) low States Fish and Wildlife Service, 1789 N. levels of genetic diversity within colonies (He = 0.109–0.357; Ho = 0.106- Wedgewood Lane, Cedar City, Utah, 84721 0.313), (2) high levels of genetic differentiation among colonies (global F = 0.296), (3) very small genetic effective population sizes, and (4) evidence Funding Information ST The work was supported by United States of genetic bottlenecks. The genetic data reveal additional subdivision such that Bureau of Land Management Challenge colonies within recovery units do not form single genotype clusters consistent Cost-Share grants, the Utah Department of with recovery unit boundaries. Genotype cluster membership support historical Natural Resources Endangered Species gene flow among colonies in the easternmost West Desert Recovery Unit with Mitigation Fund, the Utah Division of Wildlife the westernmost Pausaugunt colonies and among the eastern Pausaugunt Resources, and Syracuse University. colonies and the Awapa Recovery unit to the north. In order to maintain the long-term viability of the species, there needs to be an increased focus on main- Received: 5 March 2015; Accepted: 23 November 2015 taining suitable habitat between groups of existing populations that can act as connective corridors. The location of future translocation sites should be Ecology and Evolution 2016; 6(2): located in areas that will maximize connectivity, leading to maintenance of 426–446 genetic variation and evolutionary potential. doi: 10.1002/ece3.1874 Introduction climate change, small isolated populations are likely to experience increased extinction probabilities due to Habitat loss and range reduction are among the most reduced evolutionary potential (Peacock and Dochter- serious threats to species persistence (Dunham et al. mann 2012), which is dependent upon heritable genetic 1997; Collier et al. 2010; Nuria et al. 2012; Rogers and variation in adaptive traits (Naish and Hard 2008; Robin- Peacock 2012; Agnarsson et al. 2013; Gottelli et al. 2013; son et al. 2008; Naish et al. 2013; Olson et al. 2013). The Venturas et al. 2013). It is well appreciated that small iso- conservation genetics literature is replete with examples of lated demographic units are particularly vulnerable to habitat loss, fragmentation, and reductions in genetic random genetic drift and concomitant loss of genetic variation from a wide variety of taxa including once variation (Frankham 2005). Under scenarios of global widely dispersed species [e.g., mountain lion (Puma 426 ª 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. N. L. Brown et al. Utah prairie dog genetic diversity concolor; Ernest et al. 2003); white rhinoceros (Cera- populations face new challenges associated with global cli- totherium simum; Nielsen et al. 2008); Siberian flying mate change, strategies for the conservation of genetic squirrel (Pteromys volans; Lampila et al. 2009); European resources must include consideration of evolutionary ground squirrels (Spermophilus citellus; Ben Slimen et al. potential in addition to maintenance of ESU-based coad- 2012; ] as well as narrowly distributed endemics [e.g., apted gene complexes, whose “fitness benefits” may be mouse lemur species (Microcebus spp.; Olivieri et al. tied to environments that are rapidly changing. 2008); Devils Hole pupfish (Cyprinodon diabolis; Martin In western North America, many ground-dwelling sci- et al. 2012); and bluemask darter (Etheostoma akatulo; urids including all five of the prairie dog species (Gun- Robinson et al. 2013)]. Conservation strategies for species nison’s prairie dog, Cynomys gunnisoni; white-tailed with reduced genetic variation are generally aimed at prairie dog, C. leucurus; black-tailed prairie dog, C. ludo- maximizing the maintenance of the remaining genetic vianus; Mexican prairie dog, C. mexicanus and Utah variation (Peacock et al. 2010; Ernst et al. 2013; Mondol prairie dog, C. parvidens) were the target of extensive poi- et al. 2013; Schueler et al. 2013). soning regimes in the 19th and 20th centuries. These spe- For species with distinct evolutionarily significant units cies were thought to be competitors for forage with open (ESUs) designated, the challenge is not only to maintain range livestock, and their extensive burrow systems were the coadapted gene complexes which are thought to deemed an injury risk for cattle. Ironically, recent research define each unit, but also to maximize the species-level shows that cattle preferentially graze along prairie dog genetic diversity in the face of declining population num- colony edges and use their colony centers for resting, sim- bers. ESUs have been defined in a number of ways ilar to the mutualistic relationship prairie dogs once had including Moritz’s (1994) reciprocal monophyly for with the American bison (Sierra–Corona et al. 2015). mtDNA alleles Fraser and Bernatchez (2001). However, in As a result of extermination campaigns, many of these practice, genetically differentiated populations found in once widespread species are either candidates for listing differing habitats are often grouped into distinct ESUs or are now federal or state listed as threatened or endan- whether adaptive differences have been demonstrated or gered: Franklin’s ground squirrel Spermophilus franklinii, not (Peacock and Dochtermann 2012). Fraser and Ber- Mexican prairie dog; Mohave ground squirrel Sper- natchez (2001) outline an adaptive evolutionary conserva- mophilus mohavensis, Northern Idaho ground squirrel tion approach which aims to provide a more unified Spermophilus brunneus brunneus, Townsend’s ground concept that includes both genetic and ecological consid- squirrel Urocitellus townsendii townsendii, Utah prairie erations and a more flexible species-specific approach. At dog, and Washington ground squirrel Urocitellus washing- present, the International Union for Conservation of Nat- toni (http://www.fws.gov/endangered/). ure (IUCN) guidelines for within ESUs, however they are Here we focus on declines in the Utah prairie dog and defined, management practices include reestablishing examine genetic variability in the context of evolutionary extirpated populations with individuals from the closest potential for this species under current management prac- intact populations (Hoogland et al. 2011; May et al. 2011; tices. The Utah prairie dog underwent significant declines Rosell et al. 2012). Only in cases of extensive population due to a particularly draconian pest control regime dur- loss within an ESU would recolonization of habitat with ing the 20th century. These efforts together with declines individuals from outside the ESU be considered (Halley associated with the sylvatic plague (Yersinia pestis) intro- 2011). However, in practice the mixing of gene pools duced into North America in 1899 dramatically reduced from separate ESUs is not typically undertaken (Peacock the number of individuals. In the 1920s, the number of et al. 2010; Paplinska et al. 2011). However, highly Utah prairie dog was estimated at ~95,000 individuals, depauperate gene pools may require genetic rescue such but by the 1960s the population had been reduced sub- as in the extreme case of the Florida panther (Puma con- stantially and was estimated at <3300 individuals occupy- color coryi), where fixation of deleterious alleles and ing 37 colonies in 1972 (Collier and Spillett 1973). The inbreeding depression warranted interbreeding between species currently exists in eight counties in southwest subspecies (P. c. stanleyana x P.c. coryi; Pimm et al. 2006; Utah occupying three “recovery units” delineated