Implications of Large-Effect Loci for Conservation: A Review and Case Study with Pacific Salmon.

The increasing feasibility of assembling large genomic datasets for non-model species presents both opportunities and challenges for applied conservation and management. A popular theme in recent studies is the search for large-effect loci that explain substantial portions of phenotypic variance for a key trait(s). If such loci can be linked to adaptations, 2 important questions arise: 1) Should information from these loci be used to reconfigure conservation units (CUs), even if this conflicts with overall patterns of genetic differentiation? 2) How should this information be used in viability assessments of populations and larger CUs? In this review, we address these questions in the context of recent studies of Chinook salmon and steelhead (anadromous form of rainbow trout) that show strong associations between adult migration timing and specific alleles in one small genomic region. Based on the polygenic paradigm (most traits are controlled by many genes of small effect) and genetic data available at the time showing that early-migrating populations are most closely related to nearby late-migrating populations, adult migration differences in Pacific salmon and steelhead were considered to reflect diversity within CUs rather than separate CUs. Recent data, however, suggest that specific alleles are required for early migration, and that these alleles are lost in populations where conditions do not support early-migrating phenotypes. Contrasting determinations under the US Endangered Species Act and the State of California's equivalent legislation illustrate the complexities of incorporating genomics data into CU configuration decisions. Regardless how CUs are defined, viability assessments should consider that 1) early-migrating phenotypes experience disproportionate risks across large geographic areas, so it becomes important to identify early-migrating populations that can serve as reliable sources for these valuable genetic resources; and 2) genetic architecture, especially the existence of large-effect loci, can affect evolutionary potential and adaptability.

Glacier Retreat and Pacific Salmon.

Glaciers have shaped past and present habitats for Pacific salmon (Oncorhynchus spp.) in North America. During the last glacial maximum, approximately 45% of the current North American range of Pacific salmon was covered in ice. Currently, most salmon habitat occurs in watersheds in which glacier ice is present and retreating. This synthesis examines the multiple ways that glacier retreat can influence aquatic ecosystems through the lens of Pacific salmon life cycles. We predict that the coming decades will result in areas in which salmon populations will be challenged by diminished water flows and elevated water temperatures, areas in which salmon productivity will be enhanced as downstream habitat suitability increases, and areas in which new river and lake habitat will be formed that can be colonized by anadromous salmon. Effective conservation and management of salmon habitat and populations should consider the impacts of glacier retreat and other sources of ecosystem change.

Conceptualizing Ecological Responses to Dam Removal: If You Remove It, What's to Come?

One of the desired outcomes of dam decommissioning and removal is the recovery of aquatic and riparian ecosystems. To investigate this common objective, we synthesized information from empirical studies and ecological theory into conceptual models that depict key physical and biological links driving ecological responses to removing dams. We define models for three distinct spatial domains: upstream of the former reservoir, within the reservoir, and downstream of the removed dam. Emerging from these models are response trajectories that clarify potential pathways of ecological transitions in each domain. We illustrate that the responses are controlled by multiple causal pathways and feedback loops among physical and biological components of the ecosystem, creating recovery trajectories that are dynamic and nonlinear. In most cases, short-term effects are typically followed by longer-term responses that bring ecosystems to new and frequently predictable ecological condition, which may or may not be similar to what existed prior to impoundment.

Increasing hydrologic variability threatens depleted anadromous fish populations.

Predicting effects of climate change on species and ecosystems depend on understanding responses to shifts in means (such as trends in global temperatures), but also shifts in climate variability. To evaluate potential responses of anadromous fish populations to an increasingly variable environment, we performed a hierarchical analysis of 21 Chinook salmon populations from the Pacific Northwest, examining support for changes in river flows and flow variability on population growth. More than half of the rivers analyzed have already experienced significant increases in flow variability over the last 60 years, and this study shows that this increase in variability in freshwater flows has a more negative effect than any other climate signal included in our model. Climate change models predict that this region will experience warmer winters and more variable flows, which may limit the ability of these populations to recover.

Correction: Fraik et al. The Impacts of Dam Construction and Removal on the Genetics of Recovering Steelhead (Oncorhynchus mykiss) Populations across the Elwha River Watershed. Genes 2021, 12, 89.

In the original publication [...].

Human influence on the spatial structure of threatened Pacific salmon metapopulations.

To remain viable, populations must be resilient to both natural and human-caused environmental changes. We evaluated anthropogenic effects on spatial connections among populations of Chinook salmon (Oncorhynchus tshawytscha) and steelhead (O. mykiss) (designated as threatened under the U.S. Endangered Species Act) in the lower Columbia and Willamette rivers. For several anthropogenic-effects scenarios, we used graph theory to characterize the spatial relation among populations. We plotted variance in population size against connectivity among populations. In our scenarios, reduced habitat quality decreased the size of populations and hydropower dams on rivers led to the extirpation of several populations, both of which decreased connectivity. Operation of fish hatcheries increased connectivity among populations and led to patchy or panmictic populations. On the basis of our results, we believe recolonization of the upper Cowlitz River by fall and spring Chinook and winter steelhead would best restore metapopulation structure to near-historical conditions. Extant populations that would best conserve connectivity would be those inhabiting the Molalla (spring Chinook), lower Cowlitz, or Clackamas (fall Chinook) rivers and the south Santiam (winter steelhead) and north fork Lewis rivers (summer steelhead). Populations in these rivers were putative sources; however, they were not always the most abundant or centrally located populations. This result would not have been obvious if we had not considered relations among populations in a metapopulation context. Our results suggest that dispersal rate strongly controls interactions among the populations that comprise salmon metapopulations. Thus, monitoring efforts could lead to understanding of the true rates at which wild and hatchery fish disperse. Our application of graph theory allowed us to visualize how metapopulation structure might respond to human activity. The method could be easily extended to evaluations of anthropogenic effects on other stream-dwelling populations and communities and could help prioritize among competing conservation measures.

The Impacts of Dam Construction and Removal on the Genetics of Recovering Steelhead (Oncorhynchus mykiss) Populations across the Elwha River Watershed.

Dam construction and longitudinal river habitat fragmentation disrupt important life histories and movement of aquatic species. This is especially true for Oncorhynchus mykiss that exhibits both migratory (steelhead) and non-migratory (resident rainbow) forms. While the negative effects of dams on salmonids have been extensively documented, few studies have had the opportunity to compare population genetic diversity and structure prior to and following dam removal. Here we examine the impacts of the removal of two dams on the Elwha River on the population genetics of O. mykiss. Genetic data were produced from >1200 samples collected prior to dam removal from both life history forms, and post-dam removal from steelhead. We identified three genetic clusters prior to dam removal primarily explained by isolation due to dams and natural barriers. Following dam removal, genetic structure decreased and admixture increased. Despite large O. mykiss population declines after dam construction, we did not detect shifts in population genetic diversity or allele frequencies of loci putatively involved in migratory phenotypic variation. Steelhead descendants from formerly below and above dammed populations recolonized the river rapidly after dam removal, suggesting that dam construction did not significantly reduce genetic diversity underlying O. mykiss life history strategies. These results have significant evolutionary implications for the conservation of migratory adaptive potential in O. mykiss populations above current anthropogenic barriers.

Glacier retreat creating new Pacific salmon habitat in western North America.

Glacier retreat poses risks and benefits for species of cultural and economic importance. One example is Pacific salmon (Oncorhynchus spp.), supporting subsistence harvests, and commercial and recreational fisheries worth billions of dollars annually. Although decreases in summer streamflow and warming freshwater is reducing salmon habitat quality in parts of their range, glacier retreat is creating new streams and lakes that salmon can colonize. However, potential gains in future salmon habitat associated with glacier loss have yet to be quantified across the range of Pacific salmon. Here we project future gains in Pacific salmon freshwater habitat by linking a model of glacier mass change for 315 glaciers, forced by five different Global Climate Models, with a simple model of salmon stream habitat potential throughout the Pacific Mountain ranges of western North America. We project that by the year 2100 glacier retreat will create 6,146 (±1,619) km of new streams accessible for colonization by Pacific salmon, of which 1,930 (±569) km have the potential to be used for spawning and juvenile rearing, representing 0 to 27% gains within the 18 sub-regions we studied. These findings can inform proactive management and conservation of Pacific salmon in this era of rapid climate change.

Shifting food web structure during dam removal-Disturbance and recovery during a major restoration action.

We measured food availability and diet composition of juvenile salmonids over multiple years and seasons before and during the world's largest dam removal on the Elwha River, Washington State. We conducted these measurements over three sediment-impacted sections (the estuary and two sections of the river downstream of each dam) and compared these to data collected from mainstem tributaries not directly affected by the massive amount of sediment released from the reservoirs. We found that sediment impacts from dam removal significantly reduced invertebrate prey availability, but juvenile salmon adjusted their foraging so that the amount of energy in diets was similar before and during dam removal. This general pattern was seen in both river and estuary habitats, although the mechanisms driving the change and the response differed between habitats. In the estuary, the dietary shifts were related to changes in invertebrate assemblages following a hydrological transition from brackish to freshwater caused by sediment deposition at the river's mouth. The loss of brackish invertebrate species caused fish to increase piscivory and rely on new prey sources such as plankton. In the river, energy provided to fish by Ephemeroptera, Plecoptera, and Trichoptera taxa before dam removal was replaced first by terrestrial invertebrates, and then by sediment-tolerant taxa such as Chironomidae. The results of our study are consistent with many others that have shown sharp declines in invertebrate density during dam removal. Our study further shows how those changes can move through the food web and affect fish diet composition, selectivity, and energy availability. As we move further along the dam removal response trajectory, we hypothesize that food web complexity will continue to increase as annual sediment load now approaches natural background levels, anadromous fish have recolonized the majority of the watershed between and above the former dams, and revegetation and microhabitats continue to develop in the estuary.

Large river habitat complexity and productivity of Puget Sound Chinook salmon.

While numerous studies have shown that floodplain habitat complexity can be important to fish ecology, few quantify how watershed-scale complexity influences productivity. This scale mismatch complicates population conservation and recovery strategies that evaluate recovery at regional or multi-basin scales. We used outputs from a habitat status and trends monitoring program for ten of Puget Sound's large river systems to examine whether juvenile Chinook salmon productivity relates to watershed-scale habitat complexity. We derived habitat complexity metrics that quantified wood jam densities, side and braid to main channel ratios, and node densities from a remote sensing census of Puget Sound's large river systems. Principal component analysis revealed that 91% of variance in these metrics could be explained by two principal components. These metrics revealed gradients in habitat complexity across Puget Sound which were sensitive to changes in complexity as a result of restoration actions in one watershed. Mixed effects models revealed that the second principle component term (PC2) describing habitat complexity was positively related to log transformed subyearling Chinook per spawner productivity rates from 6-18 cohorts per watershed. Total subyearling productivity (subyearlings per spawner) and fry productivity (subyearling fry per spawner) rates were best described by models that included a positive effect of habitat complexity (PC2) and negative relationships with log transformed peak flow recurrence interval, suggestive of reduced survival due to egg destruction during floods. Total subyearling productivity (subyearlings per spawner) and parr productivity (subyearling parr per spawner) rates were best described by models that included a positive effect of habitat complexity (PC2) and negative relationships with log transformed spawner density, suggestive of density dependent limits on juvenile rearing habitat. We also found that coefficient of variation for log transformed subyearling productivity and subyearling fry productivity rates declined with increasing habitat complexity, supporting the idea that habitat complexity buffers populations from annual variation in environmental conditions. Therefore, we conclude that our watershed-scale census-based approach provided habitat complexity metrics that explained some of the variability in productivity of subyearling juveniles among Chinook salmon populations. Furthermore, this approach may provide a useful means to track and evaluate aggregate effects of habitat changes on the productivity of Endangered Species Act (ESA) listed Chinook salmon populations over time.

Morphodynamic evolution following sediment release from the world's largest dam removal.

Sediment pulses can cause widespread, complex changes to rivers and coastal regions. Quantifying landscape response to sediment-supply changes is a long-standing problem in geomorphology, but the unanticipated nature of most sediment pulses rarely allows for detailed measurement of associated landscape processes and evolution. The intentional removal of two large dams on the Elwha River (Washington, USA) exposed ~30 Mt of impounded sediment to fluvial erosion, presenting a unique opportunity to quantify source-to-sink river and coastal responses to a massive sediment-source perturbation. Here we evaluate geomorphic evolution during and after the sediment pulse, presenting a 5-year sediment budget and morphodynamic analysis of the Elwha River and its delta. Approximately 65% of the sediment was eroded, of which only ~10% was deposited in the fluvial system. This restored fluvial supply of sand, gravel, and wood substantially changed the channel morphology. The remaining ~90% of the released sediment was transported to the coast, causing ~60 ha of delta growth. Although metrics of geomorphic change did not follow simple time-coherent paths, many signals peaked 1-2 years after the start of dam removal, indicating combined impulse and step-change disturbance responses.

Trends in developed land cover adjacent to habitat for threatened salmon in Puget Sound, Washington, USA.

For widely distributed species at risk, such as Pacific salmon (Oncorhynchus spp.), habitat monitoring is both essential and challenging. Only recently have widespread monitoring programs been implemented for salmon habitat in the Pacific Northwest. Remote sensing data, such as Landsat images, are therefore a useful way to evaluate trends prior to the advent of species-specific habitat monitoring programs. We used annual (1986-2008) land cover maps created from Landsat images via automated algorithms (LandTrendr) to evaluate trends in developed (50-100% impervious) land cover in areas adjacent to five types of habitat utilized by Chinook salmon (O. tshawytscha) in the Puget Sound region of Washington State, U.S.A. For the region as a whole, we found significant increases in developed land cover adjacent to each of the habitat types evaluated (nearshore, estuary, mainstem channel, tributary channel, and floodplain), but the increases were small (<1% total increase from 1986 to 2008). For each habitat type, the increasing trend changed during the time series. In nearshore, mainstem, and floodplain areas, the rate of increase in developed land cover slowed in the latter portion of the time series, while the opposite occurred in estuary and tributary areas. Watersheds that were already highly developed in 1986 tended to have higher rates of development than initially less developed watersheds. Overall, our results suggest that developed land cover in areas adjacent to Puget Sound salmon habitat has increased only slightly since 1986 and that the rate of change has slowed near some key habitat types, although this has occurred within the context of a degraded baseline condition.

Evolutionary history of Pacific salmon in dynamic environments.

Contemporary evolution of Pacific salmon (Oncorhynchus spp.) is best viewed in the context of the evolutionary history of the species and the dynamic ecosystems they inhabit. Speciation was complete by the late Miocene, leaving c. six million years for intraspecific diversification. Following the most recent glacial maximum, large areas became available for recolonization. Current intraspecific diversity is thus the product of recent evolution overlaid onto divergent historical lineages forged during recurrent episodes of Pleistocene glaciation. In northwestern North America, dominant habitat features have been relatively stable for the past 5000 years, but salmon ecosystems remain dynamic because of disturbance regimes (volcanic eruptions, landslides, wildfires, floods, variations in marine and freshwater productivity) that occur on a variety of temporal and spatial scales. These disturbances both create selective pressures for adaptive responses by salmon and inhibit long-term divergence by periodically extirpating local populations and creating episodic dispersal events that erode emerging differences. Recent anthropogenic changes are replicated pervasively across the landscape and interrupt processes that allow natural habitat recovery. If anthropogenic changes can be shaped to produce disturbance regimes that more closely mimic (in both space and time) those under which the species evolved, Pacific salmon should be well-equipped to deal with future challenges, just as they have throughout their evolutionary history.

Evolutionary consequences of habitat loss for Pacific anadromous salmonids.

Large portions of anadromous salmonid habitat in the western United States has been lost because of dams and other blockages. This loss has the potential to affect salmonid evolution through natural selection if the loss is biased, affecting certain types of habitat differentially, and if phenotypic traits correlated with those habitat types are heritable. Habitat loss can also affect salmonid evolution indirectly, by reducing genetic variation and changing its distribution within and among populations. In this paper, we compare the characteristics of lost habitats with currently accessible habitats and review the heritability of traits which show correlations with habitat/environmental gradients. We find that although there is some regional variation, inaccessible habitats tend to be higher in elevation, wetter and both warmer in the summer and colder in the winter than habitats currently available to anadromous salmonids. We present several case studies that demonstrate either a change in phenotypic or life history expression or an apparent reduction in genetic variation associated with habitat blockages. These results suggest that loss of habitat will alter evolutionary trajectories in salmonid populations and Evolutionarily Significant Units. Changes in both selective regime and standing genetic diversity might affect the ability of these taxa to respond to subsequent environmental perturbations. Both natural and anthropogenic and should be considered seriously in developing management and conservation strategies.