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We examine the evolutionary history and speculate about the evolutionary future of three basic life history ecotypes that contribute to the biocomplexity of sockeye salmon (Oncorhynchus nerka). The ‘recurrent evolution’ (RE) hypothesis claims that the sea/river ecotype is ancestral, a ‘straying’ form with poorly differentiated (meta)population structure, and that highly structured populations of lake-type sockeye and kokanee have evolved repeatedly in parallel adaptive radiations between recurrent glaciations of the Pleistocene Epoch. Basic premises of this hypothesis are consistent with new, independent evidence from recent surveys of genetic variation in mitochondrial and microsatellite DNA: (1) sockeye salmon are most closely related to pink (O. gorbuscha) and chum (O. keta) salmon with sea-type life histories; (2) the sockeye life history ecotypes exist as polyphyletic lineages within large drainages and geographic regions; (3) the sea/river ecotype exhibits less genetic differentiation among populations than the lake or kokanee ecotypes both within and among drainages; and (4) genetic diversity is typically higher in the sea/river ecotype than in the lake and kokanee ecotypes. Anthropogenic modification of estuarine habitat and intensive coastal fisheries have likely reduced and fragmented historic metapopulations of the sea/river ecotype, particularly in southern areas. In contrast, the kokanee ecotype appears to be favoured by marine fisheries and predicted changes in climate.
Biological complexity of populations is considered important for long-term sustainability of ecological goods and services. For example, the geographic and life history diversity of sockeye salmon (Oncorhynchus nerka, Walbaum, 1792) populations in Bristol Bay, Alaska have sustained a high aggregate productivity despite major changes in climatic conditions affecting the freshwater and marine environments during the last century (Hilborn et al. 2003). On the other hand, human activities increasingly threaten the persistence of such biocomplexity in the wild. Conservation decisions require scientific advice about adaptive diversity among populations – its scale and evolutionary origin, the likely evolutionary response to alternative management options, and the consequences of its loss (Wood and Gross 2008). In this paper, we examine the evolutionary origin of life history diversity in sockeye salmon, and speculate about its future in an environment that is being shaped dramatically by human society.
The species sockeye salmon comprises a multitude of reproductively isolated populations that can be grouped into three basic ecotypes based on differences in freshwater life history. The ‘lake ecotype’ is the typical anadromous form of sockeye salmon which spends about half its life in a nursery lake before migrating seaward (Burgner 1991). The ‘sea ecotype’ is also anadromous, but rears in fresh water for a shorter and more variable period (weeks or months) as it moves downstream to the estuary, typically inhabiting side channels and sloughs if these are available (Gilbert 1913). The term ‘river-type sockeye’ (Semko 1954) is sometimes used when closely spaced circuli (‘checks’) on scales indicate prolonged slow growth in fluvial or estuarine habitat. We consider the river-type form to be a special case of the sea-type life history because, by definition, neither sea-type nor river-type sockeye rear in lakes. For clarity, we will refer to them collectively as the ‘sea/river ecotype’. In contrast, the ‘kokanee ecotype’ is non-anadromous and found only in lakes (Nelson 1968).
These ecotypes exploit very different niches and exhibit corresponding adaptations. For example, common garden experiments have demonstrated that the sea/river ecotype can survive seawater at an earlier stage than the lake ecotype because of heritable differences in physiology and growth (Rice et al. 1994) and/or egg size which results in larger size and greater seawater adaptability at a given age (Wood 1995). Similar experiments with the lake and kokanee ecotypes have demonstrated heritable differences in the circannual cycle of seawater adaptability (Foote et al. 1992), gill raker morphology (Foote et al. 1999), size and age at maturity (Wood and Foote 1996), fecundity and egg size (Wood and Foote 1990, 1996), and carotenoid retention for spawning colour (Craig et al. 2005). The availability of suitable habitat varies greatly with latitude such that the sea/river ecotype is most common in glaciated rivers in northern and coastal areas of the species’ range (Wood et al. 1987; Halupka et al. 1993) whereas the kokanee ecotype is most common in southern and interior areas (Nelson 1968). The distribution of kokanee appears to be determined by lake productivity and the difficulty of anadromous migration, which in combination, likely determine fitness relative to the lake ecotype (Wood 1995). Under suitable conditions, kokanee occur sympatrically with lake-type sockeye as genetically distinct populations (Foote et al. 1989) that compete for food within the same rearing lake (Wood et al. 1999).
Wood (1995) proposed (but did not name) a ‘recurrent evolution’ (RE) hypothesis to explain the paradoxical pattern of allozyme variation in sockeye salmon. Briefly stated, sockeye salmon are presumed to have evolved as a cycle of alternating ecotypes driven by the 19 or 20 recurrent glaciations of the Pleistocene Epoch during which time each interglacial period lasted only 10 - 40 thousand years (Pielou 1991). Thus, present conditions are not typical of most of the period over which O. nerka evolved. Virtually all extant populations in Canada, southeast Alaska, and northern Washington State were established subsequent to the last glaciation which began 70–60 thousand years ago and reached its greatest extent 23–18 thousand years ago (Pielou 1991). Based on geological evidence and the geographical distribution of fish assemblages, McPhail and Lindsey (1970, 1986) concluded that Pacific salmon persisted during the last glaciation in isolated refuges in the Bering Sea region (Beringia) and south of the Cordilleran ice sheet in the Columbia River region (Cascadia). Patterns of allozyme variation in Canadian sockeye populations led Wood et al. (1994) to suggest that sockeye salmon also persisted in at least one other isolated refuge along the coast of British Columbia. This conclusion is consistent with the evidence of ‘deep structure’ in subsequent studies based on molecular markers, both in sockeye salmon (Beacham et al. 2005, 2006; Wood et al. unpubl. data, see Fig. 2), and O. kisutch (coho salmon, Smith et al. 2001), and with phylogeographic evidence in other taxa including plants (Lacourse et al. 2003) and terrestrial mammals (Byun et al. 1997).
Figure 2. Multi-dimensional scaling plot of Cavalli-Sforza and Edwards (1967) chord distance between all populations (84) with a sample size of at least 20. A - the convex hulls group populations of the same ecotype (solid squares – sea/river ecotype, open squares – lake ecotype; stars – kokanee ecotype); B – the convex hulls group populations of the same region (open circles – southern, asterisks – coastal, solid circles – northern).
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In the following paragraphs, we restate the RE hypothesis as six separate claims and review the arguments for each:
(1) The sea/river ecotype is an ancestral, ‘straying’ form of O. nerka which, like O. gorbuscha (pink salmon) and O. keta (chum salmon) typically exhibits a metapopulation1 structure. The genus Oncorhynchus evolved about 10 million years ago, likely from freshwater ancestors (McPhail 1997) although this point is open to debate (Waples et al. 2008), and speciation of O. nerka was probably complete by 7 million years ago (McKay et al. 1996; Fig. 1A). Phylogenetic studies of Pacific salmon (e.g., Stearley and Smith 1993; McKay et al. 1996; Domanico et al. 1997; Oakley and Phillips 1999) indicate that O. nerka is most closely related to O. gorbuscha and O. keta, both of which have exclusively sea-type life histories with minimal residence in fresh water after emergence. In contrast, the lake and kokanee ecotypes of O. nerka have adaptations for limnetic life (i.e., foraging on zooplankton) not seen elsewhere in the genus2 and their survival and abundance depend upon the productivity of a freshwater lake for rearing. Parsimony suggests that these limnetic adaptations evolved after O. nerka diverged from its common ancestor with O. gorbuscha and O. keta.
Figure 1. Evolution of sockeye salmon and the influence of climate change. A – Phylogeny of species in the genus Oncorhynchus and timescale for their evolution (after McKay et al. 1996). B – Trends in global temperature during the evolution of anadromous life histories in salmon and predictions for future decades (after Crowley and Kim 1995); C – Schematic niche model showing likely impact of global warming on the availability of habitat for sockeye ecotypes (modified from Wood 1995).
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(2) The sea/river ecotype is better adapted than the lake or kokanee ecotypes to persist in unproductive glaciated streams because it relies less on freshwater productivity for nutrition. Both sea-type and river-type sockeye populations currently exist where lake-type populations do not, typically in glaciated regions where lake habitat is absent or insufficiently productive (e.g., the Iskut and lower Stikine rivers, Wood et al. 1987; the East Alsek River, Geiger 2003). The sea/river ecotype is also relatively more abundant than the lake or kokanee ecotypes in many heavily glaciated drainages on the Yakutat coast of Alaska, and in northern British Columbia (Halupka et al. 1993; Wood 1995).
(3) The sea/river ecotype is better adapted than lake-type sockeye or kokanee ecotypes to colonize new freshwater habitat that becomes available as glaciers recede because of its proximity (greater persistence in glaciated habitat) and its greater tendency to stray from natal areas. Strong philopatry in lake-type sockeye appears to be a behavioral adaptation to find spawning sites that allow newly-emerged fry to reach the nursery lake despite their limited ability to overcome rapids; spawning sites are typically, but not always, situated upstream of the rearing lake (Wood 1995). This special requirement for precise homing to discrete areas of suitable spawning habitat promotes reproductive isolation and genetic differentiation of populations inhabiting even small lakes. For example, sockeye populations in six lakes in Washington State with surface areas of only 6–30 km2 were each judged sufficiently isolated and unique to be identified as distinct Evolutionarily Significant Units (Gustafson et al. 1997); similarly, sockeye populations in two small lakes (<10 km2) in British Columbia were each listed as endangered ‘wildlife species’ by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC, Irvine et al. 2005). In contrast, sea/river-type sockeye are not constrained by the discontinuous nature of lake habitat. Wood (1995) speculated from allozyme survey data that sea/river-type sockeye stray more than lake-type sockeye, and thus, might more readily colonize newly accessible freshwater habitat. However, Pavey et al. (2007) document a counter-example in which a volcanic caldera lake was colonized recently by lake-type sockeye from an adjacent drainage rather than by sea-type sockeye from downstream within the same drainage.
(4) As limnetic habitat becomes accessible and sufficiently productive following glacial retreat, specialized, locally adapted populations of lake-type sockeye evolve in a parallel adaptive radiation from the proximate sea/river type ecotype metapopulation. To our knowledge, this specific claim has not yet been tested. However, genetic surveys have revealed extensive divergence of lake-type sockeye populations within drainages colonized since the last glaciation, a ‘mosaic’ pattern that is unique among Pacific salmon (Utter et al. 1984; Wood 1995; Winans et al. 1996; Nelson et al. 2003).
(5) Where the lake environment is sufficiently productive, or the seaward migration hazardous, the fitness of non-anadromous individuals can rival or exceed that of anadromous individuals, and consequently, populations of the kokanee ecotype evolve independently from proximate (often sympatric) lake-type sockeye populations. The kokanee ecotype is known to have arisen and persisted following unsuccessful introductions of the lake ecotype (Ricker 1940; Wood 1995; Quinn et al. 1998). In at least some lakes, conditions also meet the theoretical requirements for sympatric divergence of lake and kokanee ecotypes (Wood and Foote 1996). Existing genetic evidence for the independent evolution of kokanee from lake-type sockeye within separate drainages is generally compelling, although not unequivocal (Foote et al. 1989; Taylor et al. 1996).
Despite the remarkable extent of genetic and phenotypic divergence of lake-type and kokanee populations within recently colonized drainages, surprisingly little additional divergence is evident across larger geographic scales in allozymes (Guthrie et al. 1994; Varnavskaya et al. 1994; Winans et al. 1996) or mitochondrial DNA (Bickham et al. 1995; Wood et al. unpubl. data). Regional structuring is better revealed in studies of microsatellite DNA (because of greater allelic diversity), but as in other genetic markers, more variation is evident among lakes within drainages than among drainages (Beacham et al. 2006). This population structure is unusual. In chum salmon, as expected, genetic variation is greater among continents than among regions, and greater among regions within continents than among populations within regions (Sato 2004). Why then has there not been much greater divergence among sockeye salmon populations across the species’ range, given opportunities for continued evolution spanning recurrent glaciations?
(6) Many of the locally-adapted lake-type sockeye and kokanee populations are evolutionary dead ends because they are extirpated during the next glaciation which ‘resets’ the genetic structure of the species to that characterized by relatively undifferentiated metapopulations of sea/river-type sockeye. The lake ecotype is the most abundant and genetically diverse ecotype in the current interglacial period. Presumably it flourished during previous interglacial periods too, but most of the population structure and local adaptations associated with lakes in former interglacial periods would have been lost following resurgence of the ice sheets. The RE hypothesis claims that sea/river-type sockeye persisted through these glaciations, spawning in small streams in refuges at the margin of the Cordilleran ice sheet, just as they do today on the Yakutat coast of Alaska. We suggest that sea/river-type sockeye were more abundant then, freed from competition with lake-type sockeye and intense exploitation by humans, and that they existed in geographically and demographically large, relatively homogeneous metapopulations much like pink and chum salmon do today. Spatially extensive metapopulations of sea/river-type sockeye would have been less affected by random genetic drift or selection for adaptation at small spatial scales than small, isolated lake-type populations (Gustafson and Winans 1999). Persistence of such spatially extensive gene pools within glacial refuge areas could account for the relative homogeneity of allele frequencies over large distances following post-glacial dispersal. The ensuing interglacial period would afford new opportunities for the lake-type sockeye and kokanee ecotypes to re-evolve.
For the RE hypothesis to stand, we require corroborating evidence in support of three underlying assumptions: (1) sockeye salmon ecotypes are not monophyletic, but have evolved independently in different locations; (2) the sea/river ecotype strays more than the other ecotypes, resulting in a genetic metapopulation structure similar to that in pink and chum salmon; and (3) the sea/river ecotype is ancestral to the other ecotypes in drainages that were previously glaciated. We find that all three assumptions are generally consistent with new molecular genetic data.