In a new paper in PNAS, Thompson et al. (1) examine the genetic legacy of a struggling keystone species—and the implications for a phoenix-like recovery from its genetic remnants.

For thousands of years before European contact, indigenous peoples of the Pacific Northwest of North America eagerly anticipated a critical spring event: the return migration of Chinook salmon (Oncorhynchus tshawytscha) into freshwater (Fig. 1). Early-migrating Chinook travel farther upstream than typical fall-migrating Chinook and are highly valued for their superior nutritional value and for providing an influx of protein and fat during a critical period (2). The importance of these salmon is highlighted by numerous traditional celebrations and ceremonies that mark their return. Colonizing Europeans also valued these early-returning salmon, which were heavily harvested, so much so that they began to show signs of depletion as early as the 1870s in the Columbia River (34). Early-migrating Chinook also played an important role in terrestrial ecosystems by providing predators with longer access to salmon resources and transporting marine-derived nutrients farther upstream—and earlier (3). It is safe to say that these early-migrating salmon, or “spring Chinook,” were a keystone species for peoples and ecosystems.


However, this is no longer the case. Human activities, including extensive dam construction, fishing, and water diversion for agriculture, have caused wide-spread population declines and the loss of an estimated 54% of spring Chinook populations from the contiguous United States (5). In US endangered species legislation, spring Chinook populations are usually not considered separately from fall Chinook populations within the same watershed (6). In some watersheds, struggling spring Chinook populations are not listed because their fall counterparts are abundant. Spring Chinook spend much longer in freshwater than their fall counterparts, making them more vulnerable to anthropogenic habitat alteration, especially dams that limit habitat access and change downstream temperatures and flow regimes (36). In short, a keystone species has been extirpated from much of its range—but will its extirpation be forever?


In recent years, extensive effort has been put into Chinook salmon recovery: Dams are being removed, catches are carefully regulated, and water withdrawals are closely controlled. However, the recovery of spring Chinook following these efforts will depend critically on the biological basis for early migration. If migration timing is plastic (environmentally determined or behaviorally flexible), then recovery could be extremely rapid. If migration timing is genetic, then recovery could be much slower and dependent on particulars of its genetic basis, such as how many genes and what types of alleles are involved. Theory generally predicts that the simpler the genetic basis for a trait (e.g., two alleles at a single locus) the more rapid its evolution. Yet, this very property can be a double-edged sword for recovering populations; rapid evolution during the last few centuries of disturbance might have led to the loss of simple genetic variation necessary for recovery.


Genetic Control of Migration Timing


Recent research suggests that early migration in Chinook does indeed have a simple genetic basis, strongly influenced by the gene GREB1L (78). Thompson et al. (1) advance our understanding of the role GREB1L in migration timing by collecting detailed phenotypic and genetic data, which confirm a robust association between GREB1L and migration timing. Furthermore, they show that heterozygotes exhibit intermediate summer migration timing that is unlikely to be maintained in fall-run populations.


Given these results, the potential for recovery of spring Chinook would benefit from an “evolutionary impact assessment”—how much genetic variation remains, where it is, and what are the implications for the probability and speed of recovery (6)? Thompson et al. (1) provide such an assessment for the Klamath watershed in Oregon and California, where the largest dam removal project ever (scheduled to begin in 2021) will restore access to historic spring Chinook habitats. The authors use current and historical samples, the latter from archeological excavations of indigenous fishing sites, to provide baseline assessments that inform the likelihood of restoration of former spring Chinook populations from nearby contemporary fall Chinook populations. First, they show that the contemporary association between GREB1L and migration timing was likely also present in historic Klamath spring-run populations. Second, they sampled fall Chinook from three contemporary Klamath populations and showed that the spring-run allele is currently found in all three populations: at very low frequencies in two populations (Shasta and Scott Rivers) and at higher frequencies in the river with the lowest abundances (Salmon River). The authors conclude that reevolution of spring Chinook from these fall Chinook populations and, by extension, others in the area, is unlikely. However, a recent survey of a broader geographic area (8) showed that the spring-run allele is much more common in some watersheds outside the Klamath basin, especially in parts of Oregon, Washington, and Idaho, potentially providing a source of spring-run alleles for recovery, either through natural colonization or recovery actions.


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