Loss of SNP Genetic Diversity Following Population Collapse in a Recreational Walleye (Sander Vitreus) fishery Brandon E
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1644 ARTICLE Loss of SNP genetic diversity following population collapse in a recreational walleye (Sander vitreus) fishery Brandon E. Allen, Ella Bowles, Matthew R.J. Morris, and Sean M. Rogers Abstract: Walleye (Sander vitreus) are in demand as a commercially and recreationally harvested freshwater fish in Canada. Managed populations may exhibit different phenotypic and genetic signatures from their natural counterparts. In Alberta, Canada, this fishery is recovering from population collapses attributed to intensive recreational angling. We hypothesized that historical population collapses would be associated with signatures of reduced genetic diversity. To address this question, we sampled six walleye lakes in northern Alberta, including historical tissue samples for one population, and used genotyping-by- sequencing to characterize 1081 single nucleotide polymorphisms (SNPs). Lakes were identified as unique genetic clusters except for two lakes that unexpectedly exhibited signs of genetic clustering. Using historical DNA samples, 428 homologous SNPs characterized in walleye between pre- and postpopulation collapse exhibited significant reductions in multiple estimates of genetic diversity. Collectively, our results illustrate that genotype-by-sequencing methods that integrate historical and contem- porary samples in association with managed populations provide insight into the consequences of harvest pressure causing collapse. Résumé : Les dorés jaunes (Sander vitreus) sont prisés comme poissons d’eau douce exploités de manière commerciale et sportive au Canada. Les populations gérées peuvent présenter des signatures phénotypiques et génétiques différentes de celles des populations naturelles. En Alberta (Canada), cette ressource se remet d’un effondrement de la population attribué à la pêche sportive intensive. Nous avons postulé que les effondrements de populations passés seraient associés à des signatures d’une diversité génétique réduite. Pour examiner cette question, nous avons échantillonné six lacs à dorés jaunes dans le nord de l’Alberta, incluant des échantillons de tissus historiques pour une population, et utilisé le génotypage par séquençage pour caractériser 1081 polymorphismes mononucléotidiques (SNP). Il a été établi que les lacs présentent des groupements génétiques uniques, à l’exception de deux lacs qui, contrairement aux attentes, présentent des signes de regroupement génétique. Sur la base d’échantillons d’ADN historiques, 428 SNP homologues caractérisés chez des dorés jaunes d’avant et d’après l’effondrement de populations présentent des baisses significatives dans plusieurs estimations de la diversité génétique. Collectivement, nos résultats montrent que les méthodes de génotypage par séquençage qui incorporent des échantillons historiques et modernes en association avec des populations gérées fournissent de l’information sur les conséquences de la pression de la pêche menant à For personal use only. l’effondrement. [Traduit par la Rédaction] Introduction facilitates population response to changing environments (Aitken Wildlife management strategies attempt to balance the needs et al. 2008; Hamilton and Miller 2016), new diseases (Lamaze et al. of wildlife with the needs of people using the best available sci- 2012), or adaptive growth rates (Cena et al. 2006). Characterizing ence. These strategies historically have included harvest limits patterns of genetic variation within and among populations also (Pitcher 2001), antipoaching regulations (Walker et al. 2007), or provides a means to predict whether nonrandom mating struc- breeding programs (Kleiman 1989; Leberg and Firmin 2008)in tures the populations and contributes to isolating barriers (Milligan efforts to maintain stable population abundance. The relatively et al. 1994; McCracken et al. 2001; Pearse and Crandall 2004). recent integration of genetics with conservation and manage- The integration of genetic tools in heavily managed popula- ment has provided novel molecular tools that can be used to tions presents major challenges. Managed populations often mitigate the effects of inbreeding (Hedrick and Kalinowski 2000), deviate from the population genetic expectation for natural pop- identify the genetic effects of selective harvest on populations ulations (Waples 2010, 2015). Unreported historical stocking or (Allendorf et al. 2008), and detect hybridization (Neville and supplementation can contribute to uncertainty in the expected Dunham 2011; Allen et al. 2016). Where it was once difficult to population genetic profiles (Morán et al. 1991), in addition to the Can. J. Fish. Aquat. Sci. Downloaded from cdnsciencepub.com by UNIV CALGARY on 04/10/21 implement such tools for some species (DeSalle and Amato 2004; consequences of hybridization and competitive interactions be- Segelbacher et al. 2010), newer methods of sequencing are making tween wild and stocked individuals (Araki et al. 2007; Naish et al. it possible to rapidly integrate genetics into more progressive 2007; Yau and Taylor 2013; Allen et al. 2016). These challenges may management and conservation strategies for most species. be partially circumvented by the integration of fisheries genetics Identifying genetic variation is beneficial for the long-term con- in cases where there is access to historical samples, whereby tem- servation and management of a species because such variation poral comparisons can directly test the consequences of manage- Received 24 April 2017. Accepted 17 December 2017. B.E. Allen,* E. Bowles, M.R.J. Morris,† and S.M. Rogers. Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada. Corresponding author: Brandon E. Allen (email: [email protected]). *Present address: Alberta Biodiversity Monitoring Institute, University of Alberta, CW 405 Biological Sciences Centre, Edmonton, AB T6G 2E9, Canada. †Present address: Ambrose University, 150 Ambrose Circle SW, Calgary, AB T3H 0L5, Canada. Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink. Can. J. Fish. Aquat. Sci. 75: 1644–1651 (2018) dx.doi.org/10.1139/cjfas-2017-0164 Published at www.nrcresearchpress.com/cjfas on 18 December 2017. Allen et al. 1645 Table 1. Population name, river basin, year samples were collected (Year), number of individuals sampled (N), mini- mum (MinAge) and maximum (MaxAge) age of samples, minimum (MinFL) and maximum (MaxFL) fork length (in mm), and GPS location (°N, °W) of six walleye populations in Alberta, Canada. MinFL MaxFL GPS location Population River basin Year N MinAge MaxAge (mm) (mm) (°N, °W) Gods Peace–Slave 2005 20 1 15 200 583 56.82, 114.28 Graham Peace–Slave 2004 20 20 21 475 648 56.56, 114.55 Rainbow Hay 2002 20 5 10 369 503 58.28, 119.28 Round Peace–Slave 2004 20 5 17 292 510 56.75, 114.56 Vandersteene Peace–Slave 2000 20 2 22 188 685 56.61, 114.46 Smoke Peace–Slave 2005 20 2 15 228 475 54.36, 116.94 Smoke Peace–Slave 1973 20 7 13 465 552 54.36, 116.94 ment decisions (Coltman et al. 2003; Uusi-Heikkilä et al. 2015; We had two objectives for this study. The first was to character- Haponski and Stepien 2016). ize genetic population structure and genetic diversity estimates The walleye fishery in Alberta, Canada, is an ideal system in using genome-wide SNPs. We hypothesized genetic diversity which to investigate the genetic consequences of management would vary among lakes and river basins, with lakes that have strategies. Walleye is a cool-water species that persists throughout experienced population collapse associated with reduced genetic North America, occupying around 32% of all available freshwater diversity. Alternatively, collapse may not have had an impact on habitats (Bozek et al. 2011), and were likely established in Alberta genetic diversity (Lippé et al. 2006). For example, copper redhorse during the Missourian refugium (Billington 1996). Fishing pres- (Moxostoma hubbsi) population abundance in Quebec, Canada, has sure on walleye is known to be greater in Alberta due to the decreased in response to breeding sites becoming increasingly popularity of the sport fishery and limited number of populations isolated with the construction of dams (Lippé et al. 2006). Yet, available for fishing (Sullivan 2003). This increased fishing pres- genetic diversity does persist despite low census population size sure has been hypothesized to be the main factor contributing to (Lippé et al. 2006; Labonne et al. 2016). In addition, we expect the observed collapse of several walleye populations (Post et al. populations from geographically proximate lakes to be more ge- 2002). When the Walleye Management and Recovery Plan was netically alike than lakes separated by greater distances. Our sec- implemented in 1996 (Berry 1995), 62 out of 177 water bodies ond objective was to investigate temporal changes in genetic containing walleye were designated as collapsed (<0.05 fish per diversity and length-at-age within a population that has continu- hour). The goal of the management plan was to recover and sus- ally experienced harvest over the last 40 years (1973 and 2005, tain Alberta walleye populations using an active management approximately four to eight generations) with documented popu- approach; this involved implementing a diversity of minimum lation collapses. We predicted that the genetic consequences of size and catch limits in addition to special harvest licenses. Special these processes would leave phenotypic and genetic signatures in harvest licenses