Chapter 4 Kissing Cousins: Genetic Interactions between Wild and Cultured Salmon Fred M. Utter The Fulton spawning channel on the Babine River (Area 4) is one of four constructed spawning channels designed to increase sockeye production. At 4 km long, Channel 2 is one of the largest spawning channels in the world, producing 67 million sockeye fry in 2001. While the sockeye catch in the Skeena region has increased since the spawning channels were constructed in the 1960s, wild runs of sockeye have declined significantly over this period. photo: Garth Traxler 119 Part Two, Chapter 4: Introduction “...When is a chinook salmon in Puget Sound a ‘species’ ? Are Germans in Tacoma a ‘species’ of human?....Why do ‘wild’ salmon and not hatchery salmon count (under the Endangered Species Act)?” John Carlson, Republican candidate for Governor of the State of Washington in 2000. Introduction The above questions from a public figure reflect wide-spread public concern about the state of wild and hatchery salmon - concerns that are shared by many citizens of British Columbia. Mr. Carlson’s inquiries are not frivolous. They echo frustrations about seeming over-regulation and possible defiance of common sense and are based on understandings about genetic relationships that have been widely held for the past 50 years. When I entered the workforce in the 1950s, there were five species of the genus Oncorhynchus native to the US Pacific Northwest (chinook, coho, pink, chum, and sockeye salmon), plus the Asiatic masou salmon. In addition to being distinct from one another, the five local species were understood to have variant “races” within them such as spring-run and fall-run chinook, lake-type anadromous sockeye and non-migratory kokanee, as well as even- and odd- year pink salmon. Hatchery fish and ocean ranching were seen as the salvation of fisheries because, then as now, naturally-reproducing runs were declining due to habitat degradation, harvest pressures, and (in the United States at least) upstream and downstream migratory challenges imposed by dams. Like the above-noted Germans in Tacoma (presumably contrasted with those from Seattle), fall-run chinook salmon from, say, the lower Columbia River and Puget Sound were members of a common “race”. One declining segment of that race could, it was believed, readily be replenished by surpluses from the other, especially with viable hatchery returns from both groups. Of course, given the massive translocations of these two groups that have now been documented, any possible distinction that may have existed historically must have vanished through hybridization. This essay probes changes in these understandings that have occurred since I joined the work force. First, new insights into the genetic relationships among and within Oncorhynchus species are outlined. The dynamics of genetic 120 interactions among translocated and native groups are then examined. Finally, the pertinence of this knowledge to fish culture operations in British Columbia is considered. Past and present The present era of molecular genetics began in the 1960s. The resulting understandings abundance of single-gene markers has clarified and quantified relationships of genetic within families such as the Salmonidae in a manner that was previously relationships impossible (Utter 1991). Among the consequences of using such molecular markers were a better understanding of the relatedness between and among different species, races and populations of Pacific salmon, and an expansion of Oncorhynchus to include trouts of the Pacific Rim formerly included within the genus Salmo (Figure 4-1). These revised perceptions provided a better biological basis for comparisons among these salmon and trout species. For example, anadromous rainbow trout (steelhead) are now more properly grouped as biological cousins of the anadromous Pacific salmon rather than as close relatives of Atlantic salmon. The degree of divergence among the trout species is now recognized as similar to that of the North American salmon, and clear understandings have replaced formerly confusing specific and sub-specific taxonomic relationships. Ancestral The finer genetic resolution allowed by molecular markers indicates ancestral groupings within groupings within four Pacific salmon species (Figure 4-2). These images species contrast with those of Figure 4-1 by being based primarily on frequencies of shared alleles (i.e., variant forms of single genes) rather than the more diagnostic (invariant or “fixed”) molecular genetic differences that characterize closely-related species. Nevertheless, considerable confidence can be placed in groupings such as these that reflect many variable genes (i.e., loci) as well as representative within-group sampling. The ability to project these groupings on maps is consistent with their primarily geographic character. Variable life history characteristics (e.g., run timings) provide important but secondary adaptive dimensions to geographic or ancestral group characterizations. 121 Part Two, Chapter 4: Ancestral groupings within species pink salmon, O.gorbuscha sockeye salmon, O.nerka chum salmon, O.keta Figure 4-1 chinook salmon, O.tshawytscha Consensus phylogenetic coho salmon, O.kisutch tree of Oncorhynchus based on a review of masu salmon, O.masou morphological and rainbow trout, O.mykiss molecular data (revised from Utter and redband trout, O.mykiss (subsp.) Allendorf 1994). Branch golden trout, O.mykiss (subsp.) lengths approximate relative divergences ……………., O. mykiss (subsp.) among taxa. The ……………., O. mykiss (subsp.) question mark reflects uncertainty about the Mexican golden trout, O.chrysogaster (?) supposed Mexican golden trout collection. Apache trout, O.apache Gila trout, O.gilae westslope cutthroat trout, O.clarki lewisi Lahontan cutthroat trout, O.c.henshawi coastal cutthroat trout, O.c.clarki Yellowstone cutthroat trout, O.c.bouvieri Colorado River cutthroat trout, O.c.pleuriticus greenback cutthroat trout, O.c.stomias Bonneville cutthroat trout, O.c.utah Rio Grande cutthroat trout, O.c.virginalis The detail and clarity provided by molecular genetic data are illustrated by the following example from sockeye salmon. In addition to purely resident kokanee, sockeye occur either as anadromous lake-type (the predominant life history) or anadromous stream-type populations (occurring as small groupings throughout the species’ range) that are not associated with a lake environment (Fig. 4-2D). Prior to the advent of molecular genetic markers, kokanee were often considered subspecies of anadromous sockeye salmon 122 O. nerka kennerlyi; (e.g., Robertson 1961), and the stream-type anadromous adaptation was more or less ignored. Molecular genetic data now indicate that • kokanee and anadromous populations within a lake system have a recent common ancestry distinct from ancestries in other lake systems; that is, sockeye and kokanee within most lakes are more closely related than either is to sockeye or kokanee, respectively, from other lakes (Foote et al. 1989), and • stream-type populations appear to be primary colonizers of vacant (e.g., post-glacial) habitats, and are thus most likely the key to the evolutionary future of the species (Wood 1995; Gustafson and Winans 1999). This example illustrates the critical role of molecular genetic data in lineage classification. Life history traits remain crucial attributes within the adaptive framework of a lineage, but their tendency to evolve independently among lineages makes them unreliable as primary ancestral markers (Utter et al. 1993). Adaptive The distinction among subgroups within major lineages lies near or beyond divergence the threshold of detection by molecular genetic markers. Similar frequencies within major of more or less neutral marker alleles reflect recent divergence or intermittent groups gene flow among subgroups. However, these similarities may mask important directional adaptations at other loci that distinguish subgroups and enrich the genetic diversity of the lineage. For instance, no subgroup structure was apparent from a molecular genetic survey of pink salmon populations near Juneau, Alaska (Fig. 4-3). The low index of genetic diversity (FST = .003) equated to consistently high gene flow among populations of this region, and supported a general understanding of weak regional substructure among pink salmon populations. However, genetic marking of a late upstream run in Auke Creek revealed a fine substructure (i.e., a distinct subpopulation) that persisted over at least five generations (10 years). Similar within-lineage substructures have been found in other anadromous salmonids (Hendry et al. 2000). Such revelations imply the existence of pervasive adaptive substructures within anadromous salmonid lineages. Optimizing the occupation of available or emerging habitats, these substructures apparently dissolve and re-form as habitats shift, like eddies in a stream. 123 Part Two, Chapter 4: Major population groupings Figure 4-2 Major population grouping of four species of Pacific salmon in the Pacific Northwest (Utter 2001.) B Geographically diverged stream/ocean A populations are members of a common major ancestral lineage Unclear mozaic patterns of relationships among more abundant lake populations throughout region C D A. Chinook salmon, contrasting major ancestral groupings putatively descended from Bering (dark groupings) or north Pacific (light groupings) refugia (Utter et al. 1989, 1992, 1995, Teel et al. 2000). Index of genetic diversity FST = 0.123. B.