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Riverscape Genetics Identifies Speckled Dace (Rhinichthys Osculus) Cryptic Diversity in the Klamath–Trinity Basin

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Riverscape Genetics Identifies Speckled Dace (Rhinichthys Osculus) Cryptic Diversity in the Klamath–Trinity Basin Conserv Genet DOI 10.1007/s10592-017-1027-6 RESEARCH ARTICLE Riverscape genetics identifies speckled dace (Rhinichthys osculus) cryptic diversity in the Klamath–Trinity Basin Jesse C. Wiesenfeld1,2 · Damon H. Goodman3 · Andrew P. Kinziger1 Received: 26 December 2016 / Accepted: 5 November 2017 © Springer Science+Business Media B.V., part of Springer Nature 2017 Abstract Cataloging biodiversity is of great importance is unknown. The present study highlights the importance of given that habitat destruction has dramatically increased incorporating molecular analysis into biodiversity research extinction rates. While the presence of cryptic species poses to uncover cryptic diversity. We recommend that future challenges for biodiversity assessment, molecular analysis biodiversity inventories recognize three genetically distinct has proven useful in uncovering this hidden diversity. Using groups of speckled dace in the Klamath–Trinity Basin. nuclear microsatellite markers and mitochondrial DNA we investigated the genetic structure of Klamath speckled dace Keywords Riverscape genetics · Cryptic species · (Rhinichthys osculus klamathensis), a subspecies endemic Speckled dace · Rhinichthys osculus to the Klamath–Trinity basin. Analysis of 25 sample sites within the basin uncovered cryptic diversity including three distinct genetic groups: (1) a group that is widely distributed Introduction throughout the Klamath River mainstem and its tributar- ies, (2) a group distributed in the Trinity River, the largest Biodiversity is being lost at an astonishing rate due to forces tributary to the Klamath River, and (3) a group identified associated with human population growth, habitat alteration above a 10 m waterfall in Jenny Creek, a small tributary to and global climate change (McNeely et al. 1990; Chapin the Klamath River. All groups were resolved as divergent III et al. 2000). The situation is particularly troublesome in nuclear microsatellite analysis and exhibited levels of for freshwater ecosystems, as freshwater biodiversity has divergence in mitochondrial DNA that were comparable to declined at a faster rate compared to terrestrial and marine those observed among recognized Rhinichthys species. No systems (Ricciardi and Rasmussen 1999; Jenkins 2003). physical barriers currently separate the Klamath and Trinity Freshwater ecosystems contain 0.01% of the world’s water groups and the precise mechanism that generated and main- by volume; yet these systems are inhabited by 6% of all tains the groups as distinct despite contact and hybridization described species (Dudgeon et al. 2006). Fishes are the most-studied indicators of biodiversity decline in freshwa- ter ecosystems (Moyle et al. 2011) but our knowledge and Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10592-017-1027-6) contains understanding of freshwater fish diversity, patterns of end- supplementary material, which is available to authorized users. emism, and genetic variation is limited, with considerable amounts of diversity yet to be described (Myers et al. 2000; * Jesse C. Wiesenfeld Abell et al. 2008). [email protected] With limited resources for conservation, it is vital that 1 Department of Fisheries Biology, Humboldt State ecologists are able to identify the appropriate level of con- University, One Harpst Street, Arcata, CA 95521, USA servation units for protection. Species have long been con- 2 Cramer Fish Sciences, 3300 Industrial Blvd #100 West, sidered the foundation of biodiversity (McNeely et al. 1990), Sacramento, CA 95691, USA and a standard metric to monitor environmental conditions 3 US Fish and Wildlife Service, 1655 Heindon Road, Arcata, (Noss 1990). However, with the expansion of genetic data CA 95521, USA in conservation, and the uncertainty in species designation, Vol.:(0123456789)1 3 Conserv Genet conservation managers have begun to incorporate diver- Genetic studies investigating hybridization in speckled dace sity below the taxonomic species level (i.e. subspecies, are limited, but evidence of hybridization between intro- evolutionary significant units (ESUs), distinct population duced speckled dace and relict dace (Relictus solitarius) in segments). Delimitation of fauna into definable conserva- the Great Basin has been reported (Houston et al. 2012). tion units is especially difficult for organisms that are mor- Also, Smith (1973) suggested hybridization between speck- phologically indistinguishable or cryptic (Bernardo 2011). led dace and two other species (longnose dace Rhinichthys Cryptic diversity is commonly misclassified by traditional cataractae and redside shiners Richardsonius balteatus) approaches, where two or more units are mistakenly classi- based upon morphological analyses. fied as one. With the increase in DNA-based studies, cryptic Our research investigates speckled dace in the diversity is rapidly being discovered throughout taxa and Klamath–Trinity Basin in south central Oregon and bioregions (Bickford et al. 2007; Pfenninger and Schwenk northwestern California. Due to genetic distinctiveness 2007). Once cryptic diversity has been identified by molecu- and geographic isolation, speckled dace occurring in the lar analysis, how or if it is delimited into a conservation unit, Klamath–Trinity Basin are recognized as an endemic sub- such as a “species” or an “ESU”, is controversial (Niemiller species, Klamath speckled dace (R. osculus klamathensis) et al. 2013; Murphy et al. 2015). Though the identification (Oakey et al. 2004; Pfrender et al. 2004). Klamath speck- and recognition of cryptic diversity further complicates led dace are nearly continuously distributed throughout the taxonomy and conservation management, it provides a entire Klamath–Trinity Basin and occur at high abundance more realistic picture of biodiversity and extinction risks. in many areas in the basin (Moyle 2002). While speckled An accurate accounting of cryptic diversity is essential for dace are common and native to the Klamath–Trinity Basin, identification of biodiversity hotspots, species distributions, they are absent from all adjacent coastal basins, with the and reserve design (Bickford et al. 2007; Bernardo 2011; exception of introduced populations (Moyle 2002). Piggott et al. 2011). Two studies have resolved evidence for multiple speckled Speckled dace (Rhinichthys osculus), a small (typically dace lineages within the Klamath–Trinity Basin. First, Pfren- less than 100 mm fork length) freshwater cyprinid that der et al. (2004) uncovered evidence of two highly divergent occurs throughout much of the western United States, dis- mitochondrial DNA haplotypes in the Upper Klamath River plays considerable amounts of cryptic diversity that have and hypothesized that there might be two reproductively iso- yet to be categorized (e.g., Hoekzema and Sidlauskas 2014). lated forms of speckled dace co-occurring in the region. Sec- Speckled dace inhabit a wide assortment of habitats (Moyle ond, Kinziger et al. (2011) found deep divergence in nuclear 2002) but only subtle morphological differences have been microsatellites and mitochondrial DNA between speckled recorded between speckled dace populations exhibiting dace occurring in the Trinity River system versus those from species level genetic divergence (Hoekzema and Sidlauskas the Klamath River system. While these studies suggest the 2014). Presently, speckled dace are considered to be a single, presence of multiple distinct genetic groups, the numbers wide ranging species comprised of a number of subspecies. and distributions of the previous sampling locations were There are four subspecies listed under the Endangered Spe- insufficient to provide a clear understanding of speckled dace cies Act and four subspecies considered to be of conserva- genetic structuring within the Klamath–Trinity Basin. tion concern in California (Moyle et al. 2015). In this study, we conducted a higher resolution assessment Several phylogenetic studies have undertaken the task of of speckled dace genetic structure in the Klamath–Trinity untangling the evolutionary history of speckled dace (Oakey Basin using both nuclear microsatellites and mitochondrial et al. 2004; Pfrender et al. 2004; Smith and Dowling 2008; DNA markers over a broader geographic range of sampling Ardren et al. 2010; Billman et al. 2010; Hoekzema and sites. Our objective was to identify cryptic genetic groups, Sidlauskas 2014). Molecular assessments have shown that their geographic boundaries, contact zones and levels of speckled dace represent a polyphyletic taxon containing a hybridization. Overall our analysis resolved highly complex number of undescribed taxa (Ardren et al. 2010; Hoekzema patterns of genetic structuring, including (1) resolution of and Sidlauskas 2014). In general, these studies have shown deep genetic divergence between speckled dace in the Trin- that deep genetic divergence occurs among speckled dace ity River system and the Klamath River system (hereafter isolated in separate river basins. Diversification of speckled referred to as the “Klamath” and “Trinity” groups; Fig. 1), dace, like many freshwater fishes of the American west, can (2) evidence for hybridization between the Klamath and be attributed to complex geologic and climatic processes that Trinity groups near the confluence of the Klamath and caused extended periods of isolation between basins, inter- Trinity rivers, specifically in Tish Tang Creek (TT) and the spersed with episodes of dispersal associated with drainage
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