A synthesis of senescence predictions for indeterminate growth, and support from multiple tests in wild lake trout.

Senescence-the deterioration of functionality with age-varies widely across taxa in pattern and rate. Insights into why and how this variation occurs are hindered by the predominance of laboratory-focused research on short-lived model species with determinate growth. We synthesize evolutionary theories of senescence, highlight key information gaps and clarify predictions for species with low mortality and variable degrees of indeterminate growth. Lake trout are an ideal species to evaluate predictions in the wild. We monitored individual males from two populations (1976-2017) longitudinally for changes in adult mortality (actuarial senescence) and body condition (proxy for energy balance). A cross-sectional approach (2017) compared young (ages 4-10 years) and old (18-37 years) adults for (i) phenotypic performance in body condition, and semen quality-which is related to fertility under sperm competition (reproductive senescence)-and (ii) relative telomere length (potential proxy for cellular senescence). Adult growth in these particular populations is constrained by a simplified foodweb, and our data support predictions of negligible senescence when maximum size is only slightly larger than maturation size. Negative senescence (aka reverse senescence) may occur in other lake trout populations where diet shifts allow maximum sizes to greatly exceed maturation size.

Anadromy and marine habitat use of Lake trout (Salvelinus namaycush) from the central Canadian Arctic.

Anadromy was documented in 16 lake trout, Salvelinus namaycush, from Canada's central Arctic using capture data and otolith microchemistry. For the first time, estuarine/marine habitat use was described for five individuals using acoustic telemetry. Age-at-first-migration to sea was variable (10-39 years) among individuals and most S. namaycush undertook multiple anadromous migrations within their lifetime. Telemetry data suggested that S. namaycush do not travel far into marine habitats and prefer surface waters (<2 m). These results further our collective understanding of the marine ecology of Arctic S. namaycush.

Effects of repeated daily acute heat challenge on the growth and metabolism of a cold water stenothermal fish.

Temperature is an important environmental factor influencing fish physiology that varies both spatially and temporally in ecosystems. In small north temperate zone lakes, cold water piscivores rely on nearshore prey; however, this region exceeds the optimal temperature of the foraging species during summer. To cope, piscivores make short excursions into the nearshore to feed and return to cold water to digest their meal, but the physiological impacts of these repeated acute exposures to warm water are not well understood. We exposed juvenile lake trout (Salvelinus namaycush) to treatments where they were held at ∼10°C and exposed to either 17 or 22°C for 5-10 min daily for 53 days mimicking warm-water forays. Control fish, held at an average temperature of ∼10°C but not exposed to thermal variation, consumed more food and grew slightly faster than heat challenged fish, with no clear differences in body condition, hepatosomatic index, ventricle mass, or muscle concentrations of lactate dehydrogenase and cytochrome c oxidase. Aerobic metabolic rates measured at 10°C indicated that standard metabolic rates (SMR) were similar among treatments; however, fish that were repeatedly exposed to 17°C had higher maximum metabolic rates (MMR) and aerobic scopes (AS) than control fish and those repeatedly exposed to 22°C. There were no differences in MMR or AS between fish exposed to 22°C and control fish. These results suggest that although SMR of fish are robust to repeated forays into warmer environments, MMR displays plasticity, allowing fish to be less constrained aerobically in cold water after briefly occupying warmer waters.

Life-history variation along environmental and harvest clines of a northern freshwater fish: Plasticity and adaptation.

Plasticity, local adaptation and evolutionary trade-offs drive clinal variation in traits associated with lifetime growth. Disentangling the processes and determinants that cause these traits to vary helps to understand species' responses to changing environments. This is particularly urgent for exploited populations, where size-selective harvest can induce life-history evolution. Lake trout (Salvelinus namaycush) are an exploited fish with a life history adapted to low-productivity freshwaters of northern North America, which makes them highly vulnerable to ecosystem changes and overfishing. We characterized life-history variation across a broad and diverse landscape for this iconic northern freshwater fish and evaluated whether clinal variation was consistent with hypotheses for local adaptation or growth plasticity. We estimated growth-associated traits for 90 populations exposed to a diversity of environments using a Bayesian multivariate hierarchical model. We tested for clinal variation in their somatic growth, size at maturity and reproductive allocation along environmental gradients of lake productivity, climate, prey and exploitation clines under competing hypotheses of plasticity and local adaptation. Clinal life-history variation was consistent with growth plasticity and local adaptations but not harvest-induced evolution. Variation in somatic growth was explained by exploitation, climate and prey fish occurrence. Increased exploitation, from pristine to fully exploited conditions, led to increased somatic growth (from 32 to 45 mm/year) and adult life spans, and reduced age at maturity (from 11 to 8 years). Variation in size at maturity was explained by climate and, less certainly, prey fish occurrence, while reproductive allocation was explained by evolutionary trade-offs with mortality and other traits, but not environment. Lake trout life-history variation within this range was as wide as that observed across dozens of other freshwater species. Lake trout life histories resulted from evolutionary trade-offs, growth plasticity and local adaptations along several environmental clines. Presuming a plastic response, we documented ~1.4-fold growth compensation to exploitation-lower growth compensation than observed in many freshwater fishes. These results suggest that harvested species exposed to spatially structured and diverse environments may have substantial clinal variation on different traits, but due to different processes, and this has implications for their resilience and successful management.

A Multi-Life Stage Comparison of Silver Nanoparticle Toxicity on the Early Development of Three Canadian Fish Species.

Information on the effects of silver nanoparticles (AgNPs) in fish has mostly been generated from standard laboratory species and short-term toxicity tests. However, there is significant uncertainty regarding AgNP toxicity to native species of concern in North America, particularly in northern freshwater ecosystems. We assessed the chronic toxicity of AgNPs in early life stages of three North American fish species: rainbow trout (Oncorhynchus mykiss), lake trout (Salvelinus namaycush), and northern pike (Esox lucius). Newly fertilized embryos were exposed to nominal aqueous concentrations of 0.1, 0.3, 1.0, 3.0, 10.0, or 30.0 nM AgNPs for 126 (rainbow trout), 210 (lake trout), and 25 (northern pike) days. Endpoints included cumulative developmental time (°C × day or degree-days to 50% life-stage transition), mortality, fork length, embryonic malformations, cumulative survival, and histopathology of gill and liver in larvae/alevins. The results showed life stage-specific differences in responses, with endpoints during the embryonic stage occurring more often and at lower concentrations compared to larval/alevin and juvenile stages. Sensitivities among species were highly dependent on the endpoints measured, although developmental time appeared to be the most consistent endpoint across species. At embryonic and larval/alevin stages, northern pike was the most sensitive species (lowest observable effect concentration of 0.1 nM using developmental time). Rainbow trout displayed similar responses to lake trout across multiple endpoints and therefore seems to be an adequate surrogate for trout species in ecotoxicology studies. Moreover, while mortality during individual life stages was not generally affected, the cumulative mortality across life stages was significantly affected, which highlights the importance of chronic, multi-life-stage studies. Environ Toxicol Chem 2021;40:3337-3350. © 2021 SETAC.

Among-individual diet variation within a lake trout ecotype: Lack of stability of niche use.

In a polyphenic species, differences in resource use are expected among ecotypes, and homogeneity in resource use is expected within an ecotype. Yet, using a broad resource spectrum has been identified as a strategy for fishes living in unproductive northern environments, where food is patchily distributed and ephemeral. We investigated whether specialization of trophic resources by individuals occurred within the generalist piscivore ecotype of lake trout from Great Bear Lake, Canada, reflective of a form of diversity. Four distinct dietary patterns of resource use within this lake trout ecotype were detected from fatty acid composition, with some variation linked to spatial patterns within Great Bear Lake. Feeding habits of different groups within the ecotype were not associated with detectable morphological or genetic differentiation, suggesting that behavioral plasticity caused the trophic differences. A low level of genetic differentiation was detected between exceptionally large-sized individuals and other piscivore individuals. We demonstrated that individual trophic specialization can occur within an ecotype inhabiting a geologically young system (8,000-10,000 yr BP), a lake that sustains high levels of phenotypic diversity of lake trout overall. The characterization of niche use among individuals, as done in this study, is necessary to understand the role that individual variation can play at the beginning of differentiation processes.

Temporal instability of lake charr phenotypes: Synchronicity of growth rates and morphology linked to environmental variables?

Pathways through which phenotypic variation among individuals arise can be complex. One assumption often made in relation to intraspecific diversity is that the stability or predictability of the environment will interact with expression of the underlying phenotypic variation. To address biological complexity below the species level, we investigated variability across years in morphology and annual growth increments between and within two sympatric lake charr Salvelinus namaycush ecotypes in Rush Lake, USA. A rapid phenotypic shift in body and head shape was found within a decade. The magnitude and direction of the observed phenotypic change were consistent in both ecotypes, which suggests similar pathways caused the variation over time. Over the same time period, annual growth increments declined for both lake charr ecotypes and corresponded with a consistent phenotypic shift of each ecotype. Despite ecotype-specific annual growth changes in response to winter conditions, the observed annual growth shift for both ecotypes was linked, to some degree, with variation in the environment. Particularly, a declining trend in regional cloud cover was associated with an increase of early-stage (ages 1-3) annual growth for lake charr of Rush Lake. Underlying mechanisms causing changes in growth rates and constrained morphological modulation are not fully understood. An improved knowledge of the biology hidden within the expression of phenotypic variation promises to clarify our understanding of temporal morphological diversity and instability.

Impact of supplementation on deleterious mutation distribution in an exploited salmonid.

Deleterious mutations have important implications for the evolutionary trajectories of populations. While several studies recently investigated the dynamics of deleterious mutations in wild populations, no study has yet explored the fate of deleterious mutations in a context of populations managed by supplementation. Here, based on a dataset of nine wild and 15 supplemented Lake Trout populations genotyped at 4,982 single nucleotide polymorphisms (SNP)s by means of genotype by sequencing (GBS), we explored the effect of supplementation on the frequency of putatively deleterious variants. Three main findings are consequential for the management of fish populations. First, an increase in neutral genetic diversity in stocked populations compared with unstocked ones was observed. Second, putatively deleterious mutations were more likely to be found in unstocked than in stocked populations, suggesting a lower efficiency to purge deleterious mutations in unstocked lakes. Third, a population currently used as a major source for supplementation is characterized by several fixed putatively deleterious alleles. Therefore, other source populations with lower abundance of putatively deleterious mutations should be favored as sources of supplementation. We discuss management implications of our results, especially pertaining to the joint identification of neutral and deleterious mutations that could help refining the choice of source and sink populations for supplementation in order to maximize their evolutionary potential and to limit their mutation load.

Temporal constraints on the potential role of fry odors as cues of past reproductive success for spawning lake trout.

Deciding where to reproduce is a major challenge for most animals. Many select habitats based upon cues of successful reproduction by conspecifics, such as the presence of offspring from past reproductive events. For example, some fishes select spawning habitat following odors released by juveniles whose rearing habitat overlaps with spawning habitat. However, juveniles may emigrate before adults begin to search for spawning habitat; hence, the efficacy of juvenile cues could be constrained by degradation or dissipation rates. In lake trout (Salvelinus namaycush), odors deposited by the previous year's offspring have been hypothesized to guide adults to spawning reefs. However, in most extant populations, lake trout fry emigrate from spawning reefs during the spring and adults spawn during the fall. Therefore, we postulated that the role of fry odors in guiding habitat selection might be constrained by the time between fry emigration and adult spawning. Time course chemical, physiological, and behavioral assays indicated that the odors deposited by fry likely degrade or dissipate before adults select spawning habitats. Furthermore, fry feces did not attract wild lake trout to constructed spawning reefs in Lake Huron. Taken together, our results indicate fry odors are unlikely to act as cues for lake trout searching for spawning reefs in populations whose juveniles emigrate before the spawning season, and underscore the importance of environmental constraints on social cues.

Ice age fish in a warming world: minimal variation in thermal acclimation capacity among lake trout (Salvelinus namaycush) populations.

In the face of climate change, the persistence of cold-adapted species will depend on their adaptive capacity for physiological traits within and among populations. The lake trout (Salvelinus namaycush) is a cold-adapted salmonid and a relict from the last ice age that is well suited as a model species for studying the predicted effects of climate change on coldwater fishes. We investigated the thermal acclimation capacity of upper temperature resistance and metabolism of lake trout from four populations across four acclimation temperatures. Individuals were reared from egg fertilization onward in a common environment and, at 2 years of age, were acclimated to 8, 11, 15 or 19°C. Although one population had a slightly higher maximal metabolic rate (MMR), higher metabolic scope for activity and faster metabolic recovery across all temperatures, there was no interpopulation variation for critical thermal maximum (CTM) or routine metabolic rate (RMR) or for the thermal acclimation capacity of CTM, RMR, MMR or metabolic scope. Across the four acclimation temperatures, there was a 3°C maximal increase in CTM and 3-fold increase in RMR for all populations. Above 15°C, a decline in MMR and increase in RMR resulted in sharply reduced metabolic scope for all populations acclimated at 19°C. Together, these data suggest there is limited variation among lake trout populations in thermal physiology or capacity for thermal acclimatization, and that climate change may impact lake trout populations in a similar manner across a wide geographical range. Understanding the effect of elevated temperatures on the thermal physiology of this economically and ecologically important cold-adapted species will help inform management and conservation strategies for the long-term sustainability of lake trout populations.