UC San Diego UC San Diego Previously Published Works Title Replicate divergence between and within sounds in a marine fish: the copper rockfish (Sebastes caurinus). Permalink https://escholarship.org/uc/item/3d19h627 Journal Molecular ecology, 23(3) ISSN 0962-1083 Authors Dick, S Shurin, JB Taylor, EB Publication Date 2014-02-01 DOI 10.1111/mec.12630 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Molecular Ecology (2014) 23, 575–590 doi: 10.1111/mec.12630 Replicate divergence between and within sounds in a marine fish: the copper rockfish (Sebastes caurinus) S. DICK,*† J. B. SHURIN*‡ and E. B. TAYLOR* *Department of Zoology, Biodiversity Research Centre and Beaty Biodiversity Museum, University of British Columbia, 6270 University Blvd., Vancouver, BC V6T 1Z4, Canada, †Stantec Consulting Limited, Suite 500, 4370 Dominion Street, Burnaby, BC, V5G 4L7, Canada, ‡Division of Biological Sciences, University of California-San Diego, 9500 Gilman Dr. La Jolla, San Diego, CA 92093, USA Abstract Understanding the factors that influence larval dispersal and connectivity among mar- ine populations is critical to the conservation and sustainable management of marine resources. We assessed genetic subdivision among ten populations of copper rockfish (Sebastes caurinus) representing paired samples of outer coast and the heads of inlets in five replicate sounds on the west coast of Vancouver Island, British Columbia, using F F = P < 17 microsatellite DNA loci. Overall, subdivision ( ST) was low ( ST 0.031, 0.001), F = but consistently higher between paired coast and head of inlet sites (mean ST 0.047, P < F = À P > 0.001) compared to among the five coast sites (mean ST 0.001, 0.5) or F = P < among the five head of inlet sites (mean ST 0.026, 0.001). Heterozygosity, allelic richness and estimates of effective population size were also lower in head of inlet sites than in coast sites. Bayesian analysis identified two genetic groups across all sam- ples, a single genetic group among only coast samples, two genetic groups among head of inlet samples and two genetic groups within each sound analysed separately. Head of inlet copper rockfish tended to be shorter with lower condition factors and grew more slowly than coast sites fish. Reduced physical connectivity and selection against immigrants in contrasting outer coast–head of inlet environments likely contribute to the evolution of population structure of copper rockfish. Based on genetic connectivity, coast sites appear to be better served by existing marine protected areas than are head of inlet sites. Keywords: connectivity, dispersal, marine protected areas, population structure, Scorpaenidae, seascape genetics Received 24 September 2013; revision received 30 November 2013; accepted 2 December 2013 the study of seascape genetics has lagged behind Introduction genetic studies in the terrestrial realm (Selkoe et al. The study of landscape genetics focuses on the role of 2008; Manel & Holderegger 2013). From the limited habitat features (topography, distance, environmental studies in seascape genetics, it is evident that in addi- gradients) in structuring patterns of genetic variation tion to history (e.g. McCusker & Bentzen 2010) and within and among localities (e.g. Manel et al. 2003; natural selection (e.g. Nielsen et al. 2009), contempo- Holderegger & Wagner 2010). While the same pro- rary features of the seascape such as coastline shape, cesses (drift, differential selection and barriers to bathymetry and circulation can heavily influence the migration) influence genetic variation in all habitats, structure of natural populations (e.g. Banks et al. 2007). Such factors, however, need not act indepen- Correspondence: Eric B. Taylor, Fax: +1 604-822-2416; E-mail: dently. For instance, physical features of coastlines or [email protected] island chains can create physical retention zones that © 2013 John Wiley & Sons Ltd 576 S.DICK,J.B.SHURINandE.B.TAYLOR influence connectivity and also, through their influence areas (and, in particular, Rockfish Conservation Areas on water temperature and salinity, help to create envi- in Canada, DFO 2007; Segelbacher et al. 2010). ronmental gradients that generate distinct selective One of the prominent features of the coast of BC, regimes that may influence population structure (e.g. unlike most other areas of the range of copper rockfish, Johanessonn & Andre 2006; Schmidt et al. 2008). is the abundance of deeply incised inlets or fjords, of The scorpionfishes or rockfishes (Pisces: Scorpaeni- which about 79 have been documented (Thomson dae) are a group of teleost fishes with about 418 spe- 1981). These inlets, especially on the west coast of Van- cies, most of which are found in the Indian Ocean and couver Island in southwestern BC, have a characteristic, North Pacific Ocean (Nelson 2006). The genus Sebastes deep U-shaped basin, with a glacially derived mud bot- consists of about 107 species, all but six of which are tom. There is usually a river at the head of the inlet part of a species flock endemic to the North Pacific and an underwater ridge, or sill, at the mouth (Thom- Ocean (Johns & Avise 1998; Hyde & Vetter 2007). son 1981). The mouths of such inlets empty onto the Sebastes range from the intertidal zone to several thou- continental shelf where there is typically a seasonally sands of metres in depth, are generally long-lived and variable longshore current (Thomson 1981). Together, slow to mature (some may exceed 200 years of age) the shelf area and inlet constitute a series of ‘sounds’ and are viviparous (i.e. live-bearing). Juveniles settle in along the west coast of Vancouver Island. The topogra- rocky areas after a variable period of larval drift (gen- phy of the inlets creates unique circulation and environ- erally one to a few months, Love et al. 2002). The cop- mental gradients from the head to the mouth. For per rockfish (S. caurinus) is found in the eastern North instance, freshwater flows from rivers help to create a Pacific Ocean and ranges from the Gulf of Alaska surface outflow and a low to high surface salinity gradi- south to the Baja Peninsula where it is a common ent from head to mouth (Thomson 1981). A deeper member of the inshore rockfish assemblage from shal- inflow of high-salinity water typically occurs across the low subtidal areas to depths of about 180 m. The sill up towards the head of the inlet. These circulation inshore distribution of the copper rockfish, its docu- patterns, coupled with the partial depth constriction mented site fidelity, apparent preferences for areas of created by the sills, and the longitudinal environmental complex rocky substrate coupled with its viviparous gradients within the inlets, may have a large influence mode of reproduction and relatively short larval dura- on the extent of genetic exchange between populations tion (two-three months) may predispose it to develop- of marine organisms whose distributions encompass ment of substantial population subdivision due to both the inlets themselves and the adjacent continental limited gene flow. In fact, Buonaccorsi et al. (2002) shelf. In addition, differential selection pressures at examined microsatellite DNA variation at six loci the head and the mouth of inlets may present the possi- across six localities and documented significant popula- bility for local adaptation to also promote genetic tion subdivision, particularly between the semi- isolation. enclosed waters of Puget Sound, Washington, and In this study, we conducted a test of the idea that the coastal samples from British Columbia (BC), Oregon inlet—outer coast seascape transition influences rockfish and California, where FST was about ten times higher population structure by sampling copper rockfish from than among all coastal samples. Similarly, a major paired head of inlet and outer coast sites in five repli- genetic distinction at microsatellite loci occurred cate sounds on the west coast of Vancouver Island, BC between samples taken from the semi-enclosed waters (Fig. 1). Owing to the major physical and environmental of the Strait of Georgia and outside waters (west coast differences between head of inlet sites and their adja- of Vancouver Island) in the yelloweye rockfish (S. rub- cent outer coast (continental shelf) areas, we predicted errimus, Siegle et al. 2013). Taken together, these and that genetic differentiation would be most pronounced related studies suggest that coastline complexity and between these areas, followed by differences among the potential for local retention zones to form owing to samples from the heads of different inlets. Further, the interaction between topography, circulation and life given the pronounced longshore currents that occur history may be a major factor driving population sub- along the continental shelf, we expected that fish sam- division in nearshore marine fishes and in rockfishes pled from adjacent outer coast areas would be much in particular (e.g. see also Burford et al. 2011; Hess less genetically differentiated from one another. We also et al. 2011). If this is true, then marine fish population measured length, weight and age of fish to assess structure may be predictable based on geographical growth rates in copper rockfish in different habitats. features that influence dispersal. In addition, under- Differences in growth may reflect differences in the standing how the seascape influences connectivity, selective environments of the outer coast and the heads dispersal, and population structure and demography of inlets, or among sounds, which could also promote has implications for the design of marine protected population differentiation. © 2013 John Wiley & Sons Ltd HABITAT AND GENETIC STRUCTURE IN ROCKFISH 577 Fig. 1 Copper rockfish (Sebastes caurinus) BRITISH collection locations along the west coast of Vancouver Island, British Columbia COLUMBIA QS (BC), Canada. BS, Barkley Sound; CS, Clayoquot Sound; NS, Nootka Sound; KS, Kyuquot Sound; QS, Quatsino VANCOUVER Sound. Inset shows position of Vancou- KS ISLAND ver Island (boxed area) within British YT NWT Columbia. NS BC AB North Pacific Ocean CS U.S.A.