Dylan J. Fraser

Effective/census population size ratio estimation: a compendium and appraisal

With an ecological-evolutionary perspective increasingly applied toward the conservation and management of endangered or exploited species, the genetic estimation of effective population size (Ne) has proliferated. Based on a comprehensive analysis of empirical literature from the past two decades, we asked: (i) how often do studies link Ne to the adult census population size (N)? (ii) To what extent is Ne correctly linked to N? (iii) How readily is uncertainty accounted for in both Ne and N when quantifying Ne/N ratios? and (iv) how frequently and to what degree might errors in the estimation of Ne or N affect inferences of Ne/N ratios? We found that only 20% of available Ne estimates (508 of 2617; 233 studies) explicitly attempted to link Ne and N; of these, only 31% (160 of 508) correctly linked Ne and N. Moreover, only 7% (41 of 508) of Ne/N ratios (correctly linked or not) reported confidence intervals for both Ne and N; for those cases where confidence intervals were reported for Ne only, 31% of Ne/N ratios overlapped with 1, of which more than half also reached below Ne/N = 0.01. Uncertainty in Ne/N ratios thus sometimes spanned at least two orders of magnitude. We conclude that the estimation of Ne/N ratios in natural populations could be significantly improved, discuss several options for doing so, and briefly outline some future research directions.

Integrating Traditional and Evolutionary Knowledge in Biodiversity Conservation: a Population Level Case Study

Despite their dual importance in the assessment of endangered/threatened species, there have been few attempts to integrate traditional ecological knowledge (TEK) and evolutionary biology knowledge (EBK) at the population level. We contrasted long-term aboriginal TEK with previously obtained EBK in the context of seasonal migratory habits and population biology of a salmonid fish, brook charr, ( Salvelinus fontinalis) inhabiting a large, remote postglacial lake. Compilation of TEK spanning four decades involved analytical workshops, semidirective interviews, and collaborative fieldwork with local aboriginal informants and fishing guides. We found that TEK complemented EBK of brook charr by providing concordant and additional information about (1) population viability; (2) breeding areas and migration patterns of divergent populations; and (3) the behavioral ecology of populations within feeding areas; all of which may ultimately affect the maintenance of population diversity. Aboriginal concerns related to human pressures on this species, not revealed by EBK, also help to focus future conservation initiatives for divergent populations and to encourage restoration of traditional fishing practices. However, relative to EBK, the relevance of TEK to salmonid biodiversity conservation was evident mainly at a smaller spatial scale, for example, that of individual rivers occupied by populations or certain lake sectors. Nevertheless, EBK was only collected over a 4-yr period, so TEK provided an essential long-term temporal window to evaluate population differences and persistence. We concluded that, despite different conceptual underpinnings, spatially and temporally varying TEK and EBK both contribute to the knowledge base required to achieve sustainability and effective biodiversity conservation planning for a given species. Such integration may be particularly relevant in many isolated regions, where intraspecific diversity can go unrecognized due to sparse scientific knowledge or undocumented TEK, and where governmental agencies and local communities increasingly seek to find common ground on which to address biodiversity issues.

Prevalence and recurrence of escaped farmed Atlantic salmon (Salmo salar) in eastern North American rivers

Knowledge of the prevalence of escaped farmed fishes in the wild is an essential first step to assessing the risk resulting from interactions between farmed and wild fishes. This is especially important in eastern North America, where Atlantic salmon (Salmo salar) aquaculture occurs near wild Atlantic salmon rivers and where many wild salmon popula- tions are severely depressed. Here, we review the literature on the incidence of escaped farmed salmon in eastern North American rivers, for which there has been no comprehensive compilation to date. Escaped farmed salmon have been found in 54 of 62 (87%) rivers investigated within a 300 km radius of the aquaculture industry since 1984, including 11 rivers that contain endangered salmon populations. Averaged among all investigations, the proportional representation of farmed salmon among adults entering the rivers from the sea was 9.2% (range 0% to 100%). Where data were sufficient to exam- ine temporal trends, farmed salmon proportions varied considerably over time, suggesting that escape events are episodic in nature. We conclude that escaped farmed salmon are sufficiently prevalent in eastern North American rivers to pose a potentially serious risk to the persistence of wild salmon populations, especially in those rivers that are adjacent to existing aquaculture sites.

Differences in transcription levels among wild, domesticated, and hybrid Atlantic salmon (Salmo salar) from two environments

Escaped domesticated individuals can introduce disadvantageous traits into wild populations due to both adaptive differences between population ancestors and human‐induced changes during domestication. In contrast to their domesticated counterparts, some endangered wild Atlantic salmon populations encounter during their marine stage large amounts of suspended sediments, which may act as a selective agent. We used microarrays to elucidate quantitative transcriptional differences between a domesticated salmon strain, a wild population and their first‐generation hybrids during their marine life stage, to describe transcriptional responses to natural suspended sediments, and to test for adaptive genetic variation in plasticity relating to a history of natural exposure or nonexposure to suspended sediments. We identified 67 genes differing in transcription level among salmon groups. Among these genes, processes related to energy metabolism and ion homoeostasis were over‐represented, while genes contributing to immunity and actin‐/myosin‐related processes were also involved in strain differentiation. Domestic–wild hybrids exhibited intermediate transcription patterns relative to their parents for two‐thirds of all genes that differed between their parents; however, genes deviating from additivity tended to have similar levels to those expressed by the wild parent. Sediments induced increases in transcription levels of eight genes, some of which are known to contribute to external or intracellular damage mitigation. Although genetic variation in plasticity did not differ significantly between groups after correcting for multiple comparisons, two genes (metallothionein and glutathione reductase) tended to be more plastic in response to suspended sediments in wild and hybrid salmon, and merit further examination as candidate genes under natural selection.

Ecological and evolutionary patterns of freshwater maturation in Pacific and Atlantic salmonines

Reproductive tactics and migratory strategies in Pacific and Atlantic salmonines are inextricably linked through the effects of migration (or lack thereof) on age and size at maturity. In this review, we focus on the ecological and evolutionary patterns of freshwater maturation in salmonines, a key process resulting in the diversification of their life histories. We demonstrate that the energetics of maturation and reproduction provides a unifying theme for understanding both the proximate and ultimate causes of variation in reproductive schedules among species, populations, and the sexes. We use probabilistic maturation reaction norms to illustrate how variation in individual condition, in terms of body size, growth rate, and lipid storage, influences the timing of maturation. This useful framework integrates both genetic and environmental contributions to conditional strategies for maturation and, in doing so, demonstrates how flexible life histories can be both heritable and subject to strong environmental influences. We review evidence that the propensity for freshwater maturation in partially anadromous species is predictable across environmental gradients at geographic and local spatial scales. We note that growth is commonly associated with the propensity for freshwater maturation, but that life-history responses to changes in growth caused by temperature may be strikingly different than changes caused by differences in food availability. We conclude by exploring how contemporary management actions can constrain or promote the diversity of maturation phenotypes in Pacific and Atlantic salmonines and caution against underestimating the role of freshwater maturing forms in maintaining the resiliency of these iconic species.

Relative risks of inbreeding and outbreeding depression in the wild in endangered salmon

Conservation biologists routinely face the dilemma of keeping small, fragmented populations isolated, wherein inbreeding depression may ensue, or mixing such populations, which may exacerbate population declines via outbreeding depression. The joint evaluation of inbreeding and outbreeding risks in the wild cannot be readily conducted in endangered species, so a suggested ‘safe’ strategy is to mix ecologically and genetically similar populations. To evaluate this strategy, we carried out a reciprocal transplant experiment involving three neighboring populations of endangered Atlantic salmon (Salmo salar) now bred in captivity and maintained in captive and wild environments. Pure, inbred, and outbred (first and second generation) cross types were released and recaptured in the wild to simultaneously test for local adaptation, inbreeding depression, and outbreeding depression. We found little evidence of inbreeding depression after one generation of inbreeding and little evidence of either heterosis or outbreeding depression via genetic incompatibilities after one or two generations of outbreeding. A trend for outbreeding depression via the loss of local adaptation was documented in one of three populations. The effects of inbreeding were not significantly different from the effects of outbreeding. Hence, at the geographic scale evaluated (34–50 km), inbreeding for one generation and outbreeding over two generations may have similar effects on the persistence of small populations. The results further suggested that outbreeding outcomes may be highly variable or unpredictable at small genetic distances. Our work highlights the necessity of evaluating the relative costs of inbreeding and outbreeding in the conservation and management of endangered species on a case‐by‐case basis.

Concurrent habitat and life history influences on effective/census population size ratios in stream‐dwelling trout

Lower effective sizes (Ne) than census sizes (N) are routinely documented in natural populations, but knowledge of how multiple factors interact to lower Ne/N ratios is often limited. We show how combined habitat and life-history influences drive a 2.4- to 6.1-fold difference in Ne/N ratios between two pristine brook trout (Salvelinus fontinalis) populations occupying streams separated by only 750 m. Local habitat features, particularly drainage area and stream depth, govern trout biomass produced in each stream. They also generate higher trout densities in the shallower stream by favoring smaller body size and earlier age-at-maturity. The combination of higher densities and reduced breeding site availability in the shallower stream likely leads to more competition among breeding trout, which results in greater variance in individual reproductive success and a greater reduction in Ne relative to N. A similar disparity between juvenile or adult densities and breeding habitat availability is reported for other species and hence may also result in divergent Ne/N ratios elsewhere. These divergent Ne/N ratios between adjacent populations are also an instructive reminder for species conservation programs that genetic and demographic parameters may differ dramatically within species.

Population size, habitat fragmentation, and the nature of adaptive variation in a stream fish

Whether and how habitat fragmentation and population size jointly affect adaptive genetic variation and adaptive population differentiation are largely unexplored. Owing to pronounced genetic drift, small, fragmented populations are thought to exhibit reduced adaptive genetic variation relative to large populations. Yet fragmentation is known to increase variability within and among habitats as population size decreases. Such variability might instead favour the maintenance of adaptive polymorphisms and/or generate more variability in adaptive differentiation at smaller population size. We investigated these alternative hypotheses by analysing coding-gene, single-nucleotide polymorphisms associated with different biological functions in fragmented brook trout populations of variable sizes. Putative adaptive differentiation was greater between small and large populations or among small populations than among large populations. These trends were stronger for genetic population size measures than demographic ones and were present despite pronounced drift in small populations. Our results suggest that fragmentation affects natural selection and that the changes elicited in the adaptive genetic composition and differentiation of fragmented populations vary with population size. By generating more variable evolutionary responses, the alteration of selective pressures during habitat fragmentation may affect future population persistence independently of, and perhaps long before, the effects of demographic and genetic stochasticity are manifest.

Are heritability and selection related to population size in nature? Meta-analysis and conservation implications

It is widely thought that small populations should have less additive genetic variance and respond less efficiently to natural selection than large populations. Across taxa, we meta‐analytically quantified the relationship between adult census population size (N) and additive genetic variance (proxy: h2) and found no reduction in h2 with decreasing N; surveyed populations ranged from four to one million individuals (1735 h2 estimates, 146 populations, 83 species). In terms of adaptation, ecological conditions may systematically differ between populations of varying N; the magnitude of selection these populations experience may therefore also differ. We thus also meta‐analytically tested whether selection changes with N and found little evidence for systematic differences in the strength, direction or form of selection with N across different trait types and taxa (7344 selection estimates, 172 populations, 80 species). Collectively, our results (i) indirectly suggest that genetic drift neither overwhelms selection more in small than in large natural populations, nor weakens adaptive potential/h2 in small populations, and (ii) imply that natural populations of varying sizes experience a variety of environmental conditions, without consistently differing habitat quality at small N. However, we caution that the data are currently insufficient to determine whether some small populations may retain adaptive potential definitively. Further study is required into (i) selection and genetic variation in completely isolated populations of known N, under‐represented taxonomic groups, and nongeneralist species, (ii) adaptive potential using multidimensional approaches and (iii) the nature of selective pressures for specific traits.

Maternal and paternal effects on fitness correlates in outbred and inbred Atlantic salmon (Salmo salar)

Small populations are at risk of fitness reductions due to inbreeding depression and the loss of within-population genetic diversity. Although this risk can be mitigated by interpopulation outbreeding, any increases in genetic variability may be offset by reductions in fitness attributable to outbreeding depression. Here, we evaluate the risks of inbreeding and outbreeding by quantifying changes in survival and seven other fitness-related traits expressed in early life (e.g., specific growth rate, development time), using three small and neighbouring populations of Atlantic salmon (Salmo salar) reared under a common-garden experimental protocol. After accounting for parental (maternal and paternal) effects on several traits (which differed between pure and F1 outbred parents), we detected no significant cross type-level differences be- tween inbred and pure (non-inbred, within-population) cross types, outbred and pure cross types, or inbred and outbred cross types. The extent to which parental effects on fitness-related traits might be considered beneficial or detrimental can- not be reliably determined in the absence of information on the adaptive significance of the trait values in the local envi- ronment.