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.

Size, age, growth and site fidelity of anadromous cutthroat trout Oncorhynchus clarkii clarkii in the Salish Sea.

Pacific salmon Oncorhynchus spp. have been the focus of scientific research for over a century, but anadromous trout in this genus, in particular anadromous coastal cutthroat trout Oncorhynchus clarkii clarkii, have been neglected. Oncorhynchus clarkii clarkii occupy a diverse range of habitats including fresh water, brackish estuaries and marine water, but have a relatively small home range making them ideal for studies of behaviour and movements during ocean residency. In 2015, we sampled O. c. clarkii monthly along a small stretch of beach (47.08° N, 122.98° W) in Eld Inlet, south Puget Sound, Washington using a beach seine. We collected tissue for genetic tagging and stock identification and scales for aging from 427 O. c. clarkii, ranging in size from 118 to 478 mm fork length. Additionally, we enumerated redds in natal streams of those fish tagged to describe inter-habitat movement patterns and investigate site fidelity of juvenile and adult O. c. clarkii in the marine environment. Consistent with other anadromous salmonids, O. c. clarkii captured at our study beach exhibited rapid growth rates, particularly in spring following dispersal into the marine environment (mean ± SD = 0.61 ± 0.29 mm-d ). Genetic tag data revealed that while O. c. clarkii undergo inter-estuarine migrations, O. c. clarkii of all life stages exhibited site fidelity in the marine environment. Twenty-one percent (64/305) of sampled O. c. clarkii were recaptured at least once during the course of the study while multiple fish (n = 3) were recaptured up to five times. These results suggest that O. c. clarkii occupying south Puget Sound reside in or regularly return to a small geographic area in the nearshore environment for much of their life and therefore may be particularly vulnerable to anthropogenic disturbance (development, angling, etc.).

Tales from scales: old DNA yields insights into contemporary evolutionary processes affecting fishes.

Salmon and trout populations are suffering declines in abundance and diversity over much of their range around the Atlantic and Pacific rims as a consequence of many factors. One method of dealing with the decline has been to produce them in hatcheries but the wisdom of this approach has been hotly debated (e.g. Hilborn & Winton 1993; Waples 1999; Brannon et al. 2004). One concern is that domesticated hatchery strains will interbreed with locally adapted wild fish; but how do we study the genetic effects if the introgression might have occurred in the past? Hansen (2002) used DNA isolated from archived scales from brown trout, Salmo trutta (Fig. 1), to show that domesticated trout had, to varying degrees, genetically introgressed with wild, native trout in two Danish rivers. Extending that study, Hansen et al. (2009) have examined DNA from brown trout scales in six Danish rivers collected during historical (1927-1956) and contemporary (2000-2006) periods and from two hatchery source populations, to assess the effects of stocking nonlocal strains of hatchery trout and declining abundance on genetic diversity. Using 21 microsatellite loci, they revealed that genetic change occurred between the historic and contemporary time periods. Many populations appeared to have some low level of introgression from hatchery stocks and two populations apparently experienced high levels of introgression. Hansen et al. (2009) also showed that population structure persists in contemporary populations despite apparent admixture and migration among populations, providing evidence that the locally adapted populations have struggled against and, to some extent, resisted being overwhelmed by repeated introductions of and interbreeding with non-native, hatchery-produced conspecifics.

Broodstock History Strongly Influences Natural Spawning Success in Hatchery Steelhead (Oncorhynchus mykiss).

We used genetic parentage analysis of 6200 potential parents and 5497 juvenile offspring to evaluate the relative reproductive success of hatchery and natural steelhead (Onchorhynchus mykiss) when spawning in the wild between 2008 and 2011 in the Wenatchee River, Washington. Hatchery fish originating from two prior generation hatchery parents had <20% of the reproductive success of natural origin spawners. In contrast, hatchery females originating from a cross between two natural origin parents of the prior generation had equivalent or better reproductive success than natural origin females. Males originating from such a cross had reproductive success of 26-93% that of natural males. The reproductive success of hatchery females and males from crosses consisting of one natural origin fish and one hatchery origin fish was 24-54% that of natural fish. The strong influence of hatchery broodstock origin on reproductive success confirms similar results from a previous study of a different population of the same species and suggests a genetic basis for the low reproductive success of hatchery steelhead, although environmental factors cannot be entirely ruled out. In addition to broodstock origin, fish size, return time, age, and spawning location were significant predictors of reproductive success. Our results indicate that incorporating natural fish into hatchery broodstock is clearly beneficial for improving subsequent natural spawning success, even in a population that has a decades-long history of hatchery releases, as is the case in the Wenatchee River.

Can interbreeding of wild and artificially propagated animals be prevented by using broodstock selected for a divergent life history?

TWO STRATEGIES HAVE BEEN PROPOSED TO AVOID NEGATIVE GENETIC EFFECTS OF ARTIFICIALLY PROPAGATED INDIVIDUALS ON WILD POPULATIONS: (i) integration of wild and captive populations to minimize domestication selection and (ii) segregation of released individuals from the wild population to minimize interbreeding. We tested the efficacy of the strategy of segregation by divergent life history in a steelhead trout, Oncorhynchus mykiss, system, where hatchery fish were selected to spawn months earlier than the indigenous wild population. The proportion of wild ancestry smolts and adults declined by 10-20% over the three generations since the hatchery program began. Up to 80% of the naturally produced steelhead in any given year were hatchery/wild hybrids. Regression model selection analysis showed that the proportion of hatchery ancestry smolts was lower in years when stream discharge was high, suggesting a negative effect of flow on reproductive success of early-spawning hatchery fish. Furthermore, proportions of hybrid smolts and adults were higher in years when the number of naturally spawning hatchery-produced adults was higher. Divergent life history failed to prevent interbreeding when physical isolation was ineffective, an inadequacy that is likely to prevail in many other situations.

A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change.

Salmonine fishes are commonly subjected to strong, novel selective pressures due to anthropogenic activities and global climate change, often resulting in population extinction. Consequently, there is considerable interest in predicting the long-term evolutionary trajectories of extant populations. Knowledge of the genetic architecture of fitness traits is integral to making these predictions. We reviewed the published, peer-reviewed literature for estimates of heritability and genetic correlation for fitness traits in salmonine fishes with two broad goals in mind: summarization of published data and testing for differences among categorical variables (e.g., species, life history type, experimental conditions). Balanced coverage of variables was lacking and estimates for wild populations and behavioral traits were nearly absent. Distributions of heritability estimates were skewed toward low values and distributions of genetic correlations toward large, positive values, suggesting that significant potential for evolution of traits exists. Furthermore, experimental conditions had a direct effect on h (2) estimates, and other variables had more complex effects on h (2) and r G estimates, suggesting that available estimates may be insufficient for use in models to predict evolutionary change in wild populations. Given this and other inherent complicating factors, making accurate predictions of the evolutionary trajectories of salmonine fishes will be a difficult task.