Coding Gene Single Nucleotide Polymorphism Population Genetics of Nonnative Brook Trout: The Ghost of Introductions Past

Fish have been translocated throughout the world, and introductions often have been executed repeatedly and have used mixtures of different strains from the native range. This history might have contributed to their invasive potential by allowing introduced and invading populations to circumvent expected reductions in genetic diversity from founder effects in a scenario termed the “genetic paradox” of invasions. We characterize patterns of genetic diversity in nonnative Brook Trout Salvelinus fontinalis, which have been introduced across the western United States for over a century but have also invaded broadly and pose a primary threat to native trout. We analyzed 155 coding gene single nucleotide polymorphisms (SNPs) in 34 nonnative Brook Trout populations sampled across eight large river systems as well as samples from the only four hatchery strains with documented use in Idaho. We uncovered similar within-population genetic diversity and large effective population sizes in naturalized populations compared with hatchery samples. Naturalized populations also showed substantial genetic structuring (maximum pairwise FST = 0.23) across and even within watersheds and indicated suggestions of admixture in certain regions. Assignment probabilities confirmed two main hatcheries as the origin of most fish collected in the field; however, the four hatcheries were excluded as being the origin for 8% of individuals, mirroring results from clustering analyses and suggesting the influence of an additional unsampled hatchery source or sources. Simulated admixtures of hatchery samples produced genetic patterns similar to those observed in field samples, further supporting an influence of multiple historic hatchery stocks on the contemporary genetic structure of Brook Trout in Idaho. Our study highlights the potential contribution of historic hatchery and introduction practices in creating genetically variable and structured naturalized Brook Trout populations across Idaho, which may have allowed these fish to defy the “genetic paradox” early on in their nonnative history and set the stage for successful establishment and subsequent invasion. The application of genetic tools to understanding an invasion of nonnative species has increased greatly in recent years, and much attention has been focused on what has been termed the “genetic paradox” of invasions (Roman and Darling 2007); that is, how do introduced species establish and invade when they should have reduced genetic variability from founder effects and therefore high extinction risk and little evolutionary *Corresponding author: [email protected] Received September 4, 2012; accepted March 31, 2013 potential? Recent empirical studies of invasions have unraveled this paradox via several mechanisms. First, many studies have found invasive populations often do not have reduced genetic variation compared with native populations (e.g., Blum et al. 2007; Lavergne and Molofsky 2007). This is often attributed to large propagule sizes arising from multiple introductions (Lockwood et al. 2005; Roman 2006; Roman and 1215 D ow nl oa de d by [ U ni ve rs ite L av al ] at 1 7: 18 0 3 Se pt em be r 20 13 1216 NEVILLE AND BERNATCHEZ Darling 2007; Dlugosch and Parker 2008; Simberloff 2009). Where introductions involve different strains from across the native range, subsequent admixture of these divergent sources can have beneficial effects on fitness (Sexton et al. 2011) and can cause dramatic shifts in genetic variation, creating novel genotypes and phenotypes on which selection can act in founding populations (Roman 2006; Lavergne and Molofsky 2007). Ultimately, the “catalytic” genetic effects (Ellstrand and Schierenbeck 2000) of these dynamic processes can actually facilitate successful establishment and invasion and make invasive fronts hotspots for unique evolutionary and ecological change (Suarez and Tsutsui 2008; Facon et al. 2008). While many invasions follow unintentional introductions, nonnative fishes have been introduced purposefully and intensively throughout the world, often with catastrophic consequences for native fishes (Casal 2006; Gozlan et al. 2010). Salmonines (salmon, trout, and char) have been a particular focus of aquaculture and introduction programs to the extent that they are now one of the broadest invaders in the world (Lever 1996; Lowe et al. 2000; Dunham et al. 2004). Salmonine introductions in many cases have spanned decades, if not centuries, and often have been executed repeatedly using mixtures of different strains from the native range (Behnke 1992; Moyle 2002; Helfman 2007; Crawford and Muir 2008). Collectively, these aspects of the history of salmonine introductions may greatly facilitate the invasive potential of these fish. Here, we evaluated contemporary genetic structure in naturalized nonnative populations of Brook Trout Salvelinus fontinalis in Idaho. Brook Trout are native to the eastern and midwestern regions of North America but have been introduced across the west for over a century, where they have invaded broadly and pose a primary threat to native trout and other species (see Dunham et al. 2002, 2004; Fausch et al. 2009). In their nonnative range Brook Trout are characterized by rapid maturity and substantial reproductive plasticity, and often have high productivity and densities compared with the native species they are commonly thought to displace (Dunham et al. 2002; McGrath and Lewis 2007; Benjamin and Baxter 2010, 2012). They are highly mobile and thus are excellent upstream dispersers in small mountain streams (Gowan and Fausch 1996; Adams et al. 2000; Peterson and Fausch 2003). In many places in the mountainous west they readily invade downstream as well, and their broad-scale introduction to headwater lakes has allowed them to access otherwise unreachable habitats including headwater refugia for native trout (Adams et al. 2001; Paul and Post 2001). Their association with headwater lakes (Adams et al. 2001), as well as valley bottoms with complex habitats (Benjamin et al. 2007; Wenger et al. 2011a), helps ensure the persistence of stable source populations and has made eradication difficult. We characterized genetic patterns in this nonnative species through analysis of 155 single nucleotide polymorphisms (SNPs) identified in coding gene regions among 34 samples of Brook Trout populations across eight large river systems in Idaho. To provide insight to the potential origin of genetic diversity observed today we also analyzed samples from the only four hatchery strains documented to have been introduced in Idaho; these strains were of a broad geographic origin from across eastern North America. We integrated our evaluation of population structure and population genetic diversity with assignments of individuals to introduced strains. To our knowledge, our study is the first characterization of broad-scale genetic diversity in Brook Trout in its nonnative range.