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Genomic Signatures Among Oncorhynchus Nerka Ecotypes to Inform Conservation and Management of Endangered Sockeye Salmon

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Genomic Signatures Among Oncorhynchus Nerka Ecotypes to Inform Conservation and Management of Endangered Sockeye Salmon Received: 2 December 2015 | Accepted: 25 July 2016 DOI: 10.1111/eva.12412 ORIGINAL ARTICLE Genomic signatures among Oncorhynchus nerka ecotypes to inform conservation and management of endangered Sockeye Salmon Krista M. Nichols1 | Christine C. Kozfkay2 | Shawn R. Narum3 1Conservation Biology Division, Northwest Fisheries Science Center, National Marine Abstract Fisheries Service, NOAA, Seattle, WA, USA Conservation of life history variation is an important consideration for many species 2 Idaho Department of Fish and Game, Eagle, with trade- offs in migratory characteristics. Many salmonid species exhibit both resi- ID, USA dent and migratory strategies that capitalize on benefits in freshwater and marine en- 3Columbia River Intertribal Fish Commission, Hagerman Fish Culture Experiment Station, vironments. In this study, we investigated genomic signatures for migratory life history Hagerman, ID, USA in collections of resident and anadromous Oncorhynchus nerka (Kokanee and Sockeye Correspondence Salmon, respectively) from two lake systems, using ~2,600 SNPs from restriction- site- Krista M. Nichols, Conservation Biology associated DNA sequencing (RAD- seq). Differing demographic histories were evident Division, Northwest Fisheries Science Center, National Marine Fisheries Service, in the two systems where one pair was significantly differentiated (Redfish Lake, NOAA, Seattle, WA, USA. FST = 0.091 [95% confidence interval: 0.087 to 0.095]) but the other pair was not Email: [email protected] (Alturas Lake, FST = −0.007 [−0.008 to −0.006]). Outlier and association analyses iden- tified several candidate markers in each population pair, but there was limited evi- dence for parallel signatures of genomic variation associated with migration. Despite lack of evidence for consistent markers associated with migratory life history in this species, candidate markers were mapped to functional genes and provide evidence for adaptive genetic variation within each lake system. Life history variation has been maintained in these nearly extirpated populations ofO. nerka, and conservation efforts to preserve this diversity are important for long- term resiliency of this species. KEYWORDS migration, natural selection, random forest, residency 1 | INTRODUCTION Hohenlohe, & Allendorf, 2012; McMahon, Teeling, & Hoglund, 2014). As Shafer et al. (2015) aptly point out, there are still many uncertain- The current age of genomics provides the opportunity to investigate ties in how genomic information can be used broadly in a conserva- a more complete picture of genetic variation in natural populations tion framework, particularly for nonmodel species. However, genomic that includes signatures of adaptive variation in addition to evolu- information can address questions regarding patterns of extant genetic tionary history and connectivity (Luikart, England, Tallmon, Jordan, & diversity, how those patterns relate to environmental variables (Bragg, Taberlet, 2003). In turn, understanding the processes that have led to Supple, Andrew, & Borevitz, 2015), and whether or not potential adap- extant diversity and differentiation among populations and adapted tive genetic variation can be identified among variable ecological life ecotypes is an important consideration for restoration, conservation, history forms (Stapley et al., 2010). and management of previously extirpated, exploited, and threatened Salmonid fishes native to streams draining into the north Pacific populations (Allendorf, Hohenlohe, & Luikart, 2010; Funk, McKay, Ocean vary in timing and propensity for ocean migration as juveniles 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. Evolutionary Applications 2016; 9: 1285–1300 wileyonlinelibrary.com/journal/eva © 2016 The Authors. Evolutionary Applications | 1285 published by John Wiley & Sons Ltd 1286 | NICHOLS ET AL. and timing of return migration for spawning in their respective natal variant likely depend upon available habitat, freshwater productiv- streams (Groot & Margolis, 1991). Many species display both migra- ity (McGurk, 2000), proximity to the ocean, and difficulty of migra- tory (anadromous) and resident life histories, but differences in migra- tion (Hendry, Bohlin, Jonsson, & Berg, 2004; Wood, 1995). Multiple tory tendency and timing vary within and among species. Importantly, forms can be found sympatrically within systems, and many display these life history characters are often used as criteria for conservation genetic divergence based upon strong fidelity to spawning areas, dif- and management of populations. Previous studies have suggested ferences in spawn timing, and spawning locations (Lin, Ziegler, Quinn, that heritable variation for migration and seawater adaptation exists & Hauser, 2008; McGlauflin et al., 2011; Quinn, Stewart, & Boatright, within multiple salmonid species (see Carlson and Seamons (2008)) 2006). Genetic characterizations of sympatric forms of Kokanee and for a review), including variation between anadromous sockeye and Sockeye Salmon have found that these two life history variants are resident Kokanee Salmon (Oncorhynchus nerka; Foote, Wood, Clarke, generally more genetically similar to one another than each form is to & Blackburn, [1992]). Moreover, genetic correlations for charac- the same form in neighboring lakes (Foote, Wood, & Withler, 1989; ters related to migration vs. residency in rainbow and steelhead Taylor, Foote, & Wood, 1996; Wood & Foote, 1996). However, little trout (Oncorhynchus mykiss) suggest that there is a genetic trade- off documentation exists regarding the genetic relationship of residual between migration and residency (Hecht, Hard, Thrower, & Nichols, fish to other sympatric forms given their elusive nature (although see 2015). More recently, genomic studies have sought to evaluate molec- [Cummings, Brannon, Adams, & Thorgaard, 1997; Waples, Aebersold, ular divergence between alternative resident and migratory ecotypes & Winans, 2011]). within salmonid species in an attempt to characterize the underlying Although O. nerka as a species is not at risk for extinction, there are genetic basis for migration. For example, several studies in O. mykiss a number of isolated populations throughout the range that are locally have examined the genetic basis of migration (Hale, Thrower, Berntson, extinct or threatened (Rand et al., 2012). Including these are endan- Miller, & Nichols, 2013; Hecht, Campbell, Holecek, & Narum, 2013) or gered Snake River Sockeye Salmon in central Idaho in the Salmon River “smoltification,” the physiological process that prepares juveniles for Basin, wherein native anadromous Sockeye Salmon undertake some of migration (Hecht, Thrower, Hale, Miller, & Nichols, 2012; Nichols, Felip, the longest migrations known for the species. Until the early to middle Wheeler, & Thorgaard, 2008). Limited parallel genomic divergence has part of the 20th century, anadromous Snake River Sockeye Salmon been observed between migratory and resident forms within species populations were abundant and supported by a number of lake sys- (i.e., Pearse, Miller, Abadia- Cardoso, & Garza, 2014), but the question tems in the upper Snake and Salmon River watersheds in northeastern of whether the same or different genetic mechanisms for other species Oregon and central Idaho. These included populations returning to that vary in migration and residency is largely unexplored. the Wallowa, Payette, and the South Fork and upper Salmon rivers. In this study, we examine genetic differentiation among O. nerka To date, all but a single anadromous population found in Redfish Lake, populations that differ markedly in life history, to inform restoration on the upper Salmon River, are considered extirpated due to historical and recovery actions for this protected species. Life history variation, human activities in the watershed. The decline in population numbers within this and other species, is important in defining the discrete- led to the 1991 listing of Snake River Sockeye Salmon, under the US ness or unique properties of populations considered for conserva- Endangered Species Act (56 FR 58619 1991). At that time, a cap- tion and management policies. Four major life history variants have tive broodstock program was initiated from the 16 wild anadromous been described for O. nerka and are mainly delineated based upon the adults that returned to Redfish Lake as well as outmigrating smolts and degree of juvenile freshwater residency. There are two anadromous, residuals that were collected in the early 1990s (Kalinowski, Doornik, or migratory, life history types, whereby juveniles, born in freshwater, Kozfkay, & Waples, 2012; Kline & Flagg, 2014). Current restoration migrate to sea before returning to their natal streams to spawn. The efforts utilize the hatchery program to re- introduce Sockeye Salmon first, “anadromous lake- type,” is the most common rearing in lakes for into their native nursery lakes in the upper Salmon River Basin (Kline ~1 year before migrating to the ocean where they spend ~1–2 years & Flagg, 2014). before returning to freshwater to spawn and die (Burgner, 1991). There are three O. nerka ecological life history types in the extant Within this type, there are also creek and beach spawners (Wood, populations in the upper Salmon River. In Redfish Lake, lake- type, 1995). The second, “anadromous sea- or river type,” spends shorter
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