The crucial role of genome-wide genetic variation in conservation.

The unprecedented rate of extinction calls for efficient use of genetics to help conserve biodiversity. Several recent genomic and simulation-based studies have argued that the field of conservation biology has placed too much focus on conserving genome-wide genetic variation, and that the field should instead focus on managing the subset of functional genetic variation that is thought to affect fitness. Here, we critically evaluate the feasibility and likely benefits of this approach in conservation. We find that population genetics theory and empirical results show that conserving genome-wide genetic variation is generally the best approach to prevent inbreeding depression and loss of adaptive potential from driving populations toward extinction. Focusing conservation efforts on presumably functional genetic variation will only be feasible occasionally, often misleading, and counterproductive when prioritized over genome-wide genetic variation. Given the increasing rate of habitat loss and other environmental changes, failure to recognize the detrimental effects of lost genome-wide genetic variation on long-term population viability will only worsen the biodiversity crisis.

Temporal patterns in adult salmon migration timing across southeast Alaska.

Pacific salmon migration timing can drive population productivity, ecosystem dynamics, and human harvest. Nevertheless, little is known about long-term variation in salmon migration timing for multiple species across broad regions. We used long-term data for five Pacific salmon species throughout rapidly warming southeast Alaska to describe long-term changes in salmon migration timing, interannual phenological synchrony, relationships between climatic variation and migratory timing, and to test whether long-term changes in migration timing are related to glaciation in headwater streams. Temporal changes in the median date of salmon migration timing varied widely across species. Most sockeye populations are migrating later over time (11 of 14), but pink, chum, and especially coho populations are migrating earlier than they did historically (16 of 19 combined). Temporal trends in duration and interannual variation in migration timing were highly variable across species and populations. The greatest temporal shifts in the median date of migration timing were correlated with decreases in the duration of migration timing, suggestive of a loss of phenotypic variation due to natural selection. Pairwise interannual correlations in migration timing varied widely but were generally positive, providing evidence for weak region-wide phenological synchrony. This synchrony is likely a function of climatic variation, as interannual variation in migration timing was related to climatic phenomenon operating at large- (Pacific decadal oscillation), moderate- (sea surface temperature), and local-scales (precipitation). Surprisingly, the presence or the absence of glaciers within a watershed was unrelated to long-term shifts in phenology. Overall, there was extensive heterogeneity in long-term patterns of migration timing throughout this climatically and geographically complex region, highlighting that future climatic change will likely have widely divergent impacts on salmon migration timing. Although salmon phenological diversity will complicate future predictions of migration timing, this variation likely acts as a major contributor to population and ecosystem resiliency in southeast Alaska.

Simple life-history traits explain key effective population size ratios across diverse taxa.

Effective population size (Ne) controls both the rate of random genetic drift and the effectiveness of selection and migration, but it is difficult to estimate in nature. In particular, for species with overlapping generations, it is easier to estimate the effective number of breeders in one reproductive cycle (Nb) than Ne per generation. We empirically evaluated the relationship between life history and ratios of Ne, Nb and adult census size (N) using a recently developed model (agene) and published vital rates for 63 iteroparous animals and plants. Nb/Ne varied a surprising sixfold across species and, contrary to expectations, Nb was larger than Ne in over half the species. Up to two-thirds of the variance in Nb/Ne and up to half the variance in Ne/N was explained by just two life-history traits (age at maturity and adult lifespan) that have long interested both ecologists and evolutionary biologists. These results provide novel insights into, and demonstrate a close general linkage between, demographic and evolutionary processes across diverse taxa. For the first time, our results also make it possible to interpret rapidly accumulating estimates of Nb in the context of the rich body of evolutionary theory based on Ne per generation.

Reproductive success of jack and full-size males in a wild coho salmon population.

Despite the wealth of research on Pacific salmon Oncorhynchus spp. life histories there is limited understanding of the lifetime reproductive success of males that spend less time at sea and mature at a smaller size (jacks) than full-size males. Over half of returning male spawners can be jacks in some populations, so it is crucial to understand their contribution to population productivity. We quantified adult-to-adult reproductive success (RS) of jacks and their relative reproductive success (RRS) compared to full-size males in a wild population of coho salmon in the Auke Creek watershed, Juneau, Alaska. We used genetic data from nearly all individuals (approx. 8000) returning to spawn over a decade (2009-2019) to conduct parentage analysis and calculate individual RS. The average adult-to-adult RS of jacks (mean = 0.7 and s.e. = 0.1) was less than that of full-size males (mean = 1.1 and s.e. = 0.1). Jack RRS was consistently below 1.0 but ranged widely (0.23 to 0.96). Despite their lower average success, jacks contributed substantially to the population by siring 23% of the total returning adult offspring (1033 of 4456) produced between 2009 and 2015. Our results imply that jacks can affect evolutionary and population dynamics, and are relevant to the conservation and management of Pacific salmon.

Alternative life-history strategy contributions to effective population size in a naturally spawning salmon population.

Alternative life-history tactics are predicted to affect within-population genetic processes but have received little attention. For example, the impact of precocious males on effective population size (N e) has not been quantified directly in Pacific salmon Oncorhynchus spp., even though they can make up a large percentage of the total male spawners. We investigated the contribution of precocial males ("jacks") to N e in a naturally spawning population of Coho Salmon O. kisutch from the Auke Creek watershed in Juneau, Alaska. Mature adults that returned from 2009 to 2019 (~8000 individuals) were genotyped at 259 single-nucleotide polymorphism (SNP) loci for parentage analysis. We used demographic and genetic methods to estimate the effective number of breeders per year (N b). Jack contribution to N b was assessed by comparing values of N b calculated with and without jacks and their offspring. Over a range of N b values (108-406), the average jack contribution to N b from 2009 to 2015 was 12.9% (SE = 3.8%). Jacks consistently made up over 20% of the total male spawners. The presence of jacks did not seem to influence N b/N. The linkage disequilibrium N e estimate was lower than the demographic estimate, possibly due to immigration effects on population genetic processes: based on external marks and parentage data, we estimated that immigrant spawners produced 4.5% of all returning offspring. Our results demonstrate that jacks can influence N b and N e and can make a substantial contribution to population dynamics and conservation of threatened stocks.

Genetic change for earlier migration timing in a pink salmon population.

To predict how climate change will influence populations, it is necessary to understand the mechanisms, particularly microevolution and phenotypic plasticity, that allow populations to persist in novel environmental conditions. Although evidence for climate-induced phenotypic change in populations is widespread, evidence documenting that these phenotypic changes are due to microevolution is exceedingly rare. In this study, we use 32 years of genetic data (17 complete generations) to determine whether there has been a genetic change towards earlier migration timing in a population of pink salmon that shows phenotypic change; average migration time occurs nearly two weeks earlier than it did 40 years ago. Experimental genetic data support the hypothesis that there has been directional selection for earlier migration timing, resulting in a substantial decrease in the late-migrating phenotype (from more than 30% to less than 10% of the total abundance). From 1983 to 2011, there was a significant decrease--over threefold--in the frequency of a genetic marker for late-migration timing, but there were minimal changes in allele frequencies at other neutral loci. These results demonstrate that there has been rapid microevolution for earlier migration timing in this population. Circadian rhythm genes, however, did not show any evidence for selective changes from 1993 to 2009.

Tributyltin contamination and imposex in Alaska harbors.

We quantified imposex in file dogwinkles (Nucella lima) and tributyltin (TBT) contamination in bay mussels (Mytilus trossulus) from 10 harbors and nearby control sites throughout Alaska. We found evidence of TBT contamination in mussels from four harbors (29-54 ng TBT/g wet tissue wt). Two of these harbors now show reduced TBT contamination relative to levels found in 1987. We were able to find and collect dogwinkles from seven sites. Of these, all three dogwinkle samples from harbor sites exhibited imposex, with 36%-87.5% females affected per site. In total, six of the 10 harbors had some evidence of TBT contamination.

Effects of the landscape on boreal toad gene flow: does the pattern-process relationship hold true across distinct landscapes at the northern range margin?

Understanding the impact of natural and anthropogenic landscape features on population connectivity is a major goal in evolutionary ecology and conservation. Discovery of dispersal barriers is important for predicting population responses to landscape and environmental changes, particularly for populations at geographic range margins. We used a landscape genetics approach to quantify the effects of landscape features on gene flow and connectivity of boreal toad (Bufo boreas) populations from two distinct landscapes in south-east Alaska (Admiralty Island, ANM, and the Chilkat River Valley, CRV). We used two common methodologies for calculating resistance distances in landscape genetics studies (resistance based on least-cost paths and circuit theory). We found a strong effect of saltwater on genetic distance of CRV populations, but no landscape effects were found for the ANM populations. Our discordant results show the importance of examining multiple landscapes that differ in the variability of their features, to maximize detectability of underlying processes and allow results to be broadly applicable across regions. Saltwater serves as a physiological barrier to boreal toad gene flow and affects populations on a small geographic scale, yet there appear to be few other barriers to toad dispersal in this intact northern region.

Long-term changes in imposex frequency in file dogwinkles, Nucella lima G., and tributyltin concentrations in bay mussels, Mytilus trossulus G.

We quantified imposex in file dogwinkles (Nucella lima) and tributyltin (TBT) contamination in bay mussels (Mytilus trossulus) from a number of sites in Auke Bay, Alaska, previously studied in the late 1980s. Imposex occurrence and TBT contamination have generally declined in spatial extent and severity over time. However, high levels of TBT contamination (0.069 microg TBT/g wet tissue wt.) and imposex (100% of females affected) are still present near a large boat docking facility in the bay and deserve continued attention because of the importance of this bay to the local economy and fisheries.

The Exciting Potential and Remaining Uncertainties of Genetic Rescue.

Restoring gene flow into small, isolated populations can alleviate genetic load and decrease extinction risk (i.e., genetic rescue), yet gene flow is rarely augmented as a conservation strategy. Due to this discrepancy between opportunity and action, a recent call was made for widespread genetic rescue attempts. However, several aspects of augmenting gene flow are poorly understood, including the magnitude and duration of beneficial effects and when deleterious effects are likely to occur. We discuss the remaining uncertainties of genetic rescue in order to promote and direct future research and to hasten progress toward implementing this potentially powerful conservation strategy on a broader scale.

Environmental DNA for the enumeration and management of Pacific salmon.

Pacific salmon are a keystone resource in Alaska, generating annual revenues of well over ~US$500 million/year. Due to their anadromous life history, adult spawners distribute amongst thousands of streams, posing a huge management challenge. Currently, spawners are enumerated at just a few streams because of reliance on human counters and, rarely, sonar. The ability to detect organisms by shed tissue (environmental DNA, eDNA) promises a more efficient counting method. However, although eDNA correlates generally with local fish abundances, we do not know if eDNA can accurately enumerate salmon. Here we show that daily, and near-daily, flow-corrected eDNA rate closely tracks daily numbers of returning sockeye and coho spawners and outmigrating sockeye smolts. eDNA thus promises accurate and efficient enumeration, but to deliver the most robust numbers will need higher-resolution stream-flow data, at-least-daily sampling, and a focus on species with simple life histories, since shedding rate varies amongst jacks, juveniles, and adults.

Comparative evaluation of a new effective population size estimator based on approximate bayesian computation.

We describe and evaluate a new estimator of the effective population size (N(e)), a critical parameter in evolutionary and conservation biology. This new "SummStat" N(e) estimator is based upon the use of summary statistics in an approximate Bayesian computation framework to infer N(e). Simulations of a Wright-Fisher population with known N(e) show that the SummStat estimator is useful across a realistic range of individuals and loci sampled, generations between samples, and N(e) values. We also address the paucity of information about the relative performance of N(e) estimators by comparing the SummStat estimator to two recently developed likelihood-based estimators and a traditional moment-based estimator. The SummStat estimator is the least biased of the four estimators compared. In 32 of 36 parameter combinations investigated using initial allele frequencies drawn from a Dirichlet distribution, it has the lowest bias. The relative mean square error (RMSE) of the SummStat estimator was generally intermediate to the others. All of the estimators had RMSE > 1 when small samples (n = 20, five loci) were collected a generation apart. In contrast, when samples were separated by three or more generations and N(e) < or = 50, the SummStat and likelihood-based estimators all had greatly reduced RMSE. Under the conditions simulated, SummStat confidence intervals were more conservative than the likelihood-based estimators and more likely to include true N(e). The greatest strength of the SummStat estimator is its flexible structure. This flexibility allows it to incorporate any potentially informative summary statistic from population genetic data.

Genetic rescue to the rescue.

Genetic rescue can increase the fitness of small, imperiled populations via immigration. A suite of studies from the past decade highlights the value of genetic rescue in increasing population fitness. Nonetheless, genetic rescue has not been widely applied to conserve many of the threatened populations that it could benefit. In this review, we highlight recent studies of genetic rescue and place it in the larger context of theoretical and empirical developments in evolutionary and conservation biology. We also propose directions to help shape future research on genetic rescue. Genetic rescue is a tool that can stem biodiversity loss more than has been appreciated, provides population resilience, and will become increasingly useful if integrated with molecular advances in population genomics.

Temporal patterns of genetic variation in a salmon population undergoing rapid change in migration timing.

Though genetic diversity is necessary for population persistence in rapidly changing environments, little is known about how climate-warming influences patterns of intra-population genetic variation. For a pink salmon population experiencing increasing temperatures, we used temporal genetic data (microsatellite = 1993, 2001, 2009; allozyme = 1979, 1981, 1983) to quantify the genetic effective population size (Ne ) and genetic divergence due to differences in migration timing and to estimate whether these quantities have changed over time. We predicted that temporal trends toward earlier migration timing and a corresponding loss of phenotypic variation would decrease genetic divergence based on migration timing and Ne . We observed significant genetic divergence based on migration timing and genetic heterogeneity between early- and late-migrating fish. There was also some evidence for divergent selection between early- and late-migrating fish at circadian rhythm genes, but results varied over time. Estimates of Ne from multiple methods were large (>1200) and Ne /Nc generally exceeded 0.2. Despite shifts in migration timing and loss of phenotypic variation, there was no evidence for changes in within-population genetic divergence or Ne over the course of this study. These results suggest that in instances of population stability, genetic diversity may be resistant to climate-induced changes in migration timing.

Earlier migration timing, decreasing phenotypic variation, and biocomplexity in multiple salmonid species.

Climate-induced phenological shifts can influence population, evolutionary, and ecological dynamics, but our understanding of these phenomena is hampered by a lack of long-term demographic data. We use a multi-decade census of 5 salmonid species representing 14 life histories in a warming Alaskan stream to address the following key questions about climate change and phenology: How consistent are temporal patterns and drivers of phenology for similar species and alternative life histories? Are shifts in phenology associated with changes in phenotypic variation? How do phenological changes influence the availability of resource subsidies? For most salmonid species, life stages, and life histories, freshwater temperature influences migration timing--migration events are occurring earlier in time (mean = 1.7 days earlier per decade over the 3-5 decades), and the number of days over which migration events occur is decreasing (mean = 1.5 days per decade). Temporal trends in migration timing were not correlated with changes in intra-annual phenotypic variation, suggesting that these components of the phenotypic distribution have responded to environmental change independently. Despite commonalities across species and life histories, there was important biocomplexity in the form of disparate shifts in migration timing and variation in the environmental factors influencing migration timing for alternative life history strategies in the same population. Overall, adult populations have been stable during these phenotypic and environmental changes (λ ≈ 1.0), but the temporal availability of salmon as a resource in freshwater has decreased by nearly 30 days since 1971 due to changes in the median date of migration timing and decreases in intra-annual variation in migration timing. These novel observations advance our understanding of phenological change in response to climate warming, and indicate that climate change has influenced the ecology of salmon populations, which will have important consequences for the numerous species that depend on this resource.

Combined genetic and telemetry data reveal high rates of gene flow, migration, and long-distance dispersal potential in Arctic ringed seals (Pusa hispida).

Ringed seals (Pusa hispida) are broadly distributed in seasonally ice covered seas, and their survival and reproductive success is intricately linked to sea ice and snow. Climatic warming is diminishing Arctic snow and sea ice and threatens to endanger ringed seals in the foreseeable future. We investigated the population structure and connectedness within and among three subspecies: Arctic (P. hispida hispida), Baltic (P. hispida botnica), and Lake Saimaa (P. hispida saimensis) ringed seals to assess their capacity to respond to rapid environmental changes. We consider (a) the geographical scale of migration, (b) use of sea ice, and (c) the amount of gene flow between subspecies. Seasonal movements and use of sea ice were determined for 27 seals tracked via satellite telemetry. Additionally, population genetic analyses were conducted using 354 seals representative of each subspecies and 11 breeding sites. Genetic analyses included sequences from two mitochondrial regions and genotypes of 9 microsatellite loci. We found that ringed seals disperse on a pan-Arctic scale and both males and females may migrate long distances during the summer months when sea ice extent is minimal. Gene flow among Arctic breeding sites and between the Arctic and the Baltic Sea subspecies was high; these two subspecies are interconnected as are breeding sites within the Arctic subspecies.

When are genetic methods useful for estimating contemporary abundance and detecting population trends?

The utility of microsatellite markers for inferring population size and trend has not been rigorously examined, even though these markers are commonly used to monitor the demography of natural populations. We assessed the ability of a linkage disequilibrium estimator of effective population size (N(e) ) and a simple capture-recapture estimator of abundance (N) to quantify the size and trend of stable or declining populations (true N = 100-10,000), using simulated Wright-Fisher populations. Neither method accurately or precisely estimated abundance at sample sizes of S = 30 individuals, regardless of true N. However, if larger samples of S = 60 or 120 individuals were collected, these methods provided useful insights into abundance and trends for populations of N = 100-500. At small population sizes (N = 100 or 250), precision of the N(e) estimates was improved slightly more by a doubling of loci sampled than by a doubling of individuals sampled. In general, monitoring N(e) proved a more robust means of identifying stable and declining populations than monitoring N over most of the parameter space we explored, and performance of the N(e) estimator is further enhanced if the N(e) /N ratio is low. However, at the largest population size (N = 10,000), N estimation outperformed N(e) . Both methods generally required ≥ 5 generations to pass between sampling events to correctly identify population trend.

Background matching and color-change plasticity in colonizing freshwater sculpin populations following rapid deglaciation.

Anthropogenic-induced change is forcing organisms to shift their distributions and colonize novel habitats at an increasing rate, which leads to complex interactions among evolutionary processes. Coastrange sculpin (Cottus aleuticus) have colonized recently deglaciated streams of Glacier Bay in Alaska within the last 220 years. We examined divergence among populations in background matching coloration and tested the hypothesis that observed variation is due to morphological color plasticity. To examine how color-change plasticity has interacted with other evolutionary processes, we also determined the influence of colonization on neutral genetic diversity. We observed clinal variation in substrate-matching fish color along the chronological continuum of streams. Microsatellites provided little evidence of genetic subdivision among sculpin populations. Fish color was significantly correlated to substrate color, but was not correlated to neutral population genetic structure. Furthermore, a laboratory experiment revealed that morphological color plasticity could explain much, but not all, of the observed fish color divergence. Our study demonstrates that sculpin in Glacier Bay have colonized and adapted to recently deglaciated habitat and suggests that color change plasticity has aided in this process. This research, therefore, highlights the important role phenotypic plasticity may play in the adaptation of species to rapid climate change.

tossm: an R package for assessing performance of genetic analytical methods in a management context.

tossm (Testing of Spatial Structure Methods) is a package for testing the performance of genetic analytical methods in a management context. In the tossm package, any method developed to detect population genetic structure can be combined with a mechanism for creating management units (MUs) based on the genetic analysis. The resulting Boundary-Setting Algorithm (BSA) dictates harvest boundaries with a genetic basis. These BSAs can be evaluated with respect to how well the MUs they define meet management objectives.