Conservation Genetics of the Endangered San Francisco Bay Endemic Salt Marsh Harvest Mouse (Reithrodontomys Raviventris)

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Conservation Genetics of the Endangered San Francisco Bay Endemic Salt Marsh Harvest Mouse (Reithrodontomys Raviventris) Conserv Genet (2016) 17:1055–1066 DOI 10.1007/s10592-016-0843-4 RESEARCH ARTICLE Conservation genetics of the endangered San Francisco Bay endemic salt marsh harvest mouse (Reithrodontomys raviventris) 1 1 2 2 M. J. Statham • S. Aamoth • L. Barthman-Thompson • S. Estrella • 1,2 1,2 3 1,4 S. Fresquez • L. D. Hernandez • R. Tertes • B. N. Sacks Received: 18 September 2015 / Accepted: 11 April 2016 / Published online: 19 April 2016 Ó Springer Science+Business Media Dordrecht 2016 Abstract The salt marsh harvest mouse (SMHM, complete and substantial separation of the SMHM and Reithrodontomys raviventris) is an endangered species WHM, with no evidence of hybridization. These genetic endemic to the San Francisco Bay region of California, markers as well as the mtDNA control region also identi- USA, where habitat loss and fragmentation over the past fied a deep genetic division within the SMHM concordant century have reduced the mouse’s distribution to\25 % of with the current subspecies designations, R. r. raviventris its historical range. To aid in conservation prioritization, and R. r. halicoetes. We identified the lowest genetic we first investigated the possibility of hybridization with diversity within the southern subspecies, which inhabits a the morphologically similar western harvest mouse (WHM, much reduced and highly fragmented portion of the species R. megalotis) in areas of sympatry and developed genetic range. Morphological field identification of harvest mouse tools to differentiate the two species. We then investigated species was more successful at identifying SMHM (92 %) the phylogeography and genetic structure of the SMHM, than WHM (44 %), with a large portion of WHM being including support for currently recognized SMHM sub- incorrectly identified as SMHM. Field identification of species designations. Lastly, we evaluated the morpho- harvest mouse species in the range of the southern SMHM logical criteria currently used for the identification of subspecies was just above 50 %, indicating that current species in the field. Analyses using mtDNA cytochrome methods for morphological differentiation of species in that b sequences and 11 microsatellites from 142 mice indicated area are insufficient. Our confirmation of genetically dis- tinct SMHM subspecies highlights the importance of determining the status and genetic composition of relict Electronic supplementary material The online version of this populations in the remaining patches of marshland in the article (doi:10.1007/s10592-016-0843-4) contains supplementary material, which is available to authorized users. central San Francisco Bay where the two subspecies may occur, as well as developing better tools for the discrimi- & M. J. Statham nation of species, particularly in the range of the southern [email protected] subspecies 1 Mammalian Ecology and Conservation Unit, Veterinary Genetics Laboratory, University of California, One Shields Keywords Field identification Á Management Á Avenue/Old Davis Road, Davis, CA 95616-8744, USA Morphology Á Population subdivision Á Species 2 Suisun Marsh Unit, Bay Delta Region, California Department identification Á Subspecies of Fish and Wildlife, 2109 Arch Airport Road, Stockton, CA 95206, USA 3 Don Edwards San Francisco Bay National Wildlife Refuge, Introduction United State Fish and Wildlife Service, One Marshlands Road, Fremont, CA 94555, USA Understanding the underlying genetic architecture of a 4 Department of Population Health and Reproduction, School species facilitates preservation of genetic diversity and of Veterinary Medicine, University of California, One Shields Avenue/Old Davis Road, Davis, CA 95616-8744, maintenance of maximum evolutionary potential. The USA partitioning of genetic diversity within a species reflects its 123 1056 Conserv Genet (2016) 17:1055–1066 history (Moritz 1994; Statham et al. 2014). Recent parti- the edges of salt and brackish marshes in the San Francisco tioning can result in subpopulations with similar but non- Bay Area (Fisler 1963). Differentiating between the two identical allele frequencies, whereas longer term popula- harvest mouse species in the field requires several mor- tion subdivision can allow for greater differentiation phological measurements to assign individuals to a species through genetic drift, accumulation of novel mutations, and (Shellhammer 1984). This method often identifies local adaptation if exposed to different selective environ- ambiguous individuals of intermediate morphology, clas- ments (Hewitt 2000). The magnitude of divergence or sified as unknown harvest mouse species, which has con- population subdivision also depends in part on the sizes of tributed to speculation that the two species could be populations and the frequency of migration (Paetkau 1999). undergoing hybridization (USFWS 2013). Discrepancies Habitat destruction and fragmentation associated with regarding how personnel take measurements can result in human alterations of landscapes increasingly threaten via- assignment of the same mouse to different species. In bility of endemic species, and necessitates managing pop- addition, juvenile and sub-adult mice are especially diffi- ulations to maintain genetic diversity (Allendorf and cult to identify to species. Thus additional tools are needed Luikart 2007). The coastal salt marshes of the San Fran- to ensure accurate species assignment of harvest mice. cisco Bay Area [consisting of San Francisco Bay proper A central goal of the US Fish and Wildlife Service’s species (hereafter, San Francisco), San Pablo Bay, and Suisun Bay] recovery plan for the SMHM is to maintain genetic diversity to have been reduced and fragmented by urban and agricul- minimize the risk of inbreeding depression and enable future tural development, erosion, water management, and vege- evolution and resilience to environmental change (USFWS tation change (Shellhammer 1989; USFWS 2013). This 2013). This goal is intended to secure self-sustaining popu- fragmentation will likely be exacerbated by future sea level lations of SMHM across the geographic and ecological range, rise, which is predicted to range 50–200 cm during the as well as distinct genetic units within the species. However, twenty first century (US National Research Council 2010). no phylogeographic work has been conducted to assess The salt marshes of the San Francisco Bay Area of Cali- genetic subunits or genetic diversity within the SMHM fornia are home to five endangered species including the (Shellhammer 1989; USFWS 2013). Although two sub- endemic salt marsh harvest mouse (SMHM, Reithrodonto- species of SMHM have been described, there is no morpho- mys raviventris; USFWS 2013). The SMHM (Rodentia, logical characteristic that discretely separates them. One of the Cricetidae) is restricted to salt and brackish marshes, and is main characteristics used to distinguish between the sub- highly dependent on dense cover for predator avoidance species is the color of the ventral pelage. While many indi- (Shellhammer 1989). These mice can swim well and tolerate viduals of the southern subspecies have a striking cinnamon- high salt concentrations in their diets (Fisler 1963, 1965). colored ventral fur, others have white, which is also found in Although unverified by genetic criteria, two subspecies of the majority of individuals of the northern subspecies (Shell- SMHM are recognized. The southern subspecies (R. r. hammer 1982). Thus the validity of currently recognized raviventris) inhabits central and South San Francisco Bay, subspecies needs to be investigated with genetic data. while the northern subspecies (R. r. halicoetes) occurs in San We undertook this study to provide support to conservation Pablo and Suisun Bays (Fig. 1; Shellhammer 1989). Frag- efforts for the endangered SMHM. The objectives were to: (1) mentation and loss of[75 % of the species habitat through create genetic tools for accurate species identification; (2) reclamation of tidal areas led to the SMHM being state and assess the possibility of hybridization between SMHM and federally listed as endangered (Goals project 2000; Shell- WHM; (3) characterize population sub-division in SMHM; hammer 1982, 1989; USFWS 2013). The situation is mag- (4) characterize phylogeographic (prehistorical) patterns nified in the range of the southern subspecies where[90 % among populations, including assessment of the distinctive- of the historical habitat has been lost, with most of the ness of the currently recognized northern and southern SMHM remainder lacking in suitable high tide escape habitat subspecies (R. r. halicoetes and R. r. raviventris); and (5) (USFWS 2013). Despite being listed as endangered for over quantify and compare the genetic diversity in Suisun, San 40 years there are a number of key outstanding questions Pablo, and San Francisco bays, the three primary areas of necessary for the management of the species. habitat where the species occurs. Accurate species identification is one of the most basic requirements for population monitoring. Salt marsh harvest mouse are often difficult to identify in the field due to Materials and methods extensive sympatry with the morphologically similar western harvest mouse (WHM, R. megalotis). The WHM is Fieldwork and sampling abundant and widespread, with a range across much of the western U.S., extending into Canada and Mexico. Although We trapped 142 harvest mice for genetic sampling in the WHM is primarily a grassland species, it also inhabits 2011–2013 in three locations within each of the three bays 123 Conserv Genet
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