Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity.

Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.

Genomic signatures of thermal adaptation are associated with clinal shifts of life history in a broadly distributed frog.

Temperature is a critical driver of ectotherm life-history strategies, whereby a warmer environment is associated with increased growth, reduced longevity and accelerated senescence. Increasing evidence indicates that thermal adaptation may underlie such life-history shifts in wild populations. Single nucleotide polymorphisms (SNPs) and copy number variants (CNVs) can help uncover the molecular mechanisms of temperature-driven variation in growth, longevity and senescence. However, our understanding of these mechanisms is still limited, which reduces our ability to predict the response of non-model ectotherms to global temperature change. In this study, we examined the potential role of thermal adaptation in clinal shifts of life-history traits (i.e. life span, senescence rate and recruitment) in the Columbia spotted frog Rana luteiventris along a broad temperature gradient in the western United States. We took advantage of extensive capture-recapture datasets of 20,033 marked individuals from eight populations surveyed annually for 14-18 years to examine how mean annual temperature and precipitation influenced demographic parameters (i.e. adult survival, life span, senescence rate, recruitment and population growth). After showing that temperature was the main climatic predictor influencing demography, we used RAD-seq data (50,829 SNPs and 6,599 putative CNVs) generated for 352 individuals from 31 breeding sites to identify the genomic signatures of thermal adaptation. Our results showed that temperature was negatively associated with annual adult survival and reproductive life span and positively associated with senescence rate. By contrast, recruitment increased with temperature, promoting the long-term viability of most populations. These temperature-dependent demographic changes were associated with strong genomic signatures of thermal adaptation. We identified 148 SNP candidates associated with temperature including three SNPs located within protein-coding genes regulating resistance to cold and hypoxia, immunity and reproduction in ranids. We also identified 39 CNV candidates (including within 38 transposable elements) for which normalized read depth was associated with temperature. Our study indicates that both SNPs and structural variants are associated with temperature and could eventually be found to play a functional role in clinal shifts in senescence rate and life-history strategies in R. luteiventris. These results highlight the potential role of different sources of molecular variation in the response of ectotherms to environmental temperature variation in the context of global warming.

Thermal conditions predict intraspecific variation in senescence rate in frogs and toads.

Variation in temperature is known to influence mortality patterns in ectotherms. Even though a few experimental studies on model organisms have reported a positive relationship between temperature and actuarial senescence (i.e., the increase in mortality risk with age), how variation in climate influences the senescence rate across the range of a species is still poorly understood in free-ranging animals. We filled this knowledge gap by investigating the relationships linking senescence rate, adult lifespan, and climatic conditions using long-term capture-recapture data from multiple amphibian populations. We considered two pairs of related anuran species from the Ranidae (Rana luteiventris and Rana temporaria) and Bufonidae (Anaxyrus boreas and Bufo bufo) families, which diverged more than 100 Mya and are broadly distributed in North America and Europe. Senescence rates were positively associated with mean annual temperature in all species. In addition, lifespan was negatively correlated with mean annual temperature in all species except A. boreas In both R. luteiventris and A. boreas, mean annual precipitation and human environmental footprint both had negligible effects on senescence rates or lifespans. Overall, our findings demonstrate the critical influence of thermal conditions on mortality patterns across anuran species from temperate regions. In the current context of further global temperature increases predicted by Intergovernmental Panel on Climate Change scenarios, a widespread acceleration of aging in amphibians is expected to occur in the decades to come, which might threaten even more seriously the viability of populations and exacerbate global decline.

Hybridization alters growth and migratory life-history expression of native trout.

Human-mediated hybridization threatens many native species, but the effects of introgressive hybridization on life-history expression are rarely quantified, especially in vertebrates. We quantified the effects of non-native rainbow trout admixture on important life-history traits including growth and partial migration behavior in three populations of westslope cutthroat trout over five years. Rainbow trout admixture was associated with increased summer growth rates in all populations and decreased spring growth rates in two populations with cooler spring temperatures. These results indicate that non-native admixture may increase growth under warmer conditions, but cutthroat trout have higher growth rates during cooler periods. Non-native admixture consistently increased expression of migratory behavior, suggesting that there is a genomic basis for life-history differences between these species. Our results show that effects of interspecific hybridization on fitness traits can be the product of genotype-by-environment interactions even when there are minor differences in environmental optima between hybridizing species. These results also indicate that while environmentally mediated traits like growth may play a role in population-level consequences of admixture, strong genetic influences on migratory life-history differences between these species likely explains the continued spread of non-native hybridization at the landscape-level, despite selection against hybrids at the population-level.

Ultrasound imaging identifies life history variation in resident Cutthroat Trout.

Human activities that fragment fish habitat have isolated inland salmonid populations. This isolation is associated with loss of migratory life histories and declines in population density and abundance. Isolated populations exhibiting only resident life histories may be more likely to persist if individuals can increase lifetime reproductive success by maturing at smaller sizes or earlier ages. Therefore, accurate estimates of age and size at maturity across resident salmonid populations would improve estimates of population viability. Commonly used methods for assessing maturity such as dissection, endoscopy and hormone analysis are invasive and may disturb vulnerable populations. Ultrasound imaging is a non-invasive method that has been used to measure reproductive status across fish taxa. However, little research has assessed the accuracy of ultrasound for determining maturation status of small-bodied fish, or reproductive potential early in a species' reproductive cycle. To address these knowledge gaps, we tested whether ultrasound imaging could be used to identify maturing female Westslope Cutthroat Trout (Oncorhynchus clarkii lewisi). Our methods were accurate at identifying maturing females reared in a hatchery setting up to eight months prior to spawning, with error rates ≤ 4.0%; accuracy was greater for larger fish. We also imaged fish in a field setting to examine variation in the size of maturing females among six wild, resident populations of Westslope Cutthroat Trout in western Montana. The median size of maturing females varied significantly across populations. We observed oocyte development in females as small as 109 mm, which is smaller than previously documented for this species. Methods tested in this study will allow researchers and managers to collect information on reproductive status of small-bodied salmonids without disrupting fish during the breeding season. This information can help elucidate life history traits that promote persistence of isolated salmonid populations.

Landscape resistance mediates native fish species distribution shifts and vulnerability to climate change in riverscapes.

A broader understanding of how landscape resistance influences climate change vulnerability for many species is needed, as is an understanding of how barriers to dispersal may impact vulnerability. Freshwater biodiversity is at particular risk, but previous studies have focused on popular cold-water fishes (e.g., salmon, trout, and char) with relatively large body sizes and mobility. Those fishes may be able to track habitat change more adeptly than less mobile species. Smaller, less mobile fishes are rarely represented in studies demonstrating effects of climate change, but depending on their thermal tolerance, they may be particularly vulnerable to environmental change. By revisiting 280 sites over a 20 year interval throughout a warming riverscape, we described changes in occupancy (i.e., site extirpation and colonization probabilities) and assessed the environmental conditions associated with those changes for four fishes spanning a range of body sizes, thermal and habitat preferences. Two larger-bodied trout species exhibited small changes in site occupancy, with bull trout experiencing a 9.2% (95% CI = 8.3%-10.1%) reduction, mostly in warmer stream reaches, and westslope cutthroat trout experiencing a nonsignificant 1% increase. The small-bodied cool water slimy sculpin was originally distributed broadly throughout the network and experienced a 48.0% (95% CI = 42.0%-54.0%) reduction in site occupancy with declines common in warmer stream reaches and areas subject to wildfire disturbances. The small-bodied comparatively warmer water longnose dace primarily occupied larger streams and increased its occurrence in the lower portions of connected tributaries during the study period. Distribution shifts for sculpin and dace were significantly constrained by barriers, which included anthropogenic water diversions, natural step-pools and cascades in steeper upstream reaches. Our results suggest that aquatic communities exhibit a range of responses to climate change, and that improving passage and fluvial connectivity will be important climate adaptation tactics for conserving aquatic biodiversity.

A time-lapse photography method for monitoring salmon (Oncorhynchus spp.) passage and abundance in streams.

Accurately estimating population sizes is often a critical component of fisheries research and management. Although there is a growing appreciation of the importance of small-scale salmon population dynamics to the stability of salmon stock-complexes, our understanding of these populations is constrained by a lack of efficient and cost-effective monitoring tools for streams. Weirs are expensive, labor intensive, and can disrupt natural fish movements. While conventional video systems avoid some of these shortcomings, they are expensive and require excessive amounts of labor to review footage for data collection. Here, we present a novel method for quantifying salmon in small streams (<15 m wide, <1 m deep) that uses both time-lapse photography and video in a model-based double sampling scheme. This method produces an escapement estimate nearly as accurate as a video-only approach, but with substantially less labor, money, and effort. It requires servicing only every 14 days, detects salmon 24 h/day, is inexpensive, and produces escapement estimates with confidence intervals. In addition to escapement estimation, we present a method for estimating in-stream salmon abundance across time, data needed by researchers interested in predator--prey interactions or nutrient subsidies. We combined daily salmon passage estimates with stream specific estimates of daily mortality developed using previously published data. To demonstrate proof of concept for these methods, we present results from two streams in southwest Kodiak Island, Alaska in which high densities of sockeye salmon spawn.

Evidence of climate-induced range contractions in bull trout Salvelinus confluentus in a Rocky Mountain watershed, U.S.A.

Many freshwater fish species are considered vulnerable to stream temperature warming associated with climate change because they are ectothermic, yet there are surprisingly few studies documenting changes in distributions. Streams and rivers in the U.S. Rocky Mountains have been warming for several decades. At the same time these systems have been experiencing an increase in the severity and frequency of wildfires, which often results in habitat changes including increased water temperatures. We resampled 74 sites across a Rocky Mountain watershed 17 to 20 years after initial samples to determine whether there were trends in bull trout occurrence associated with temperature, wildfire, or other habitat variables. We found that site abandonment probabilities (0.36) were significantly higher than colonization probabilities (0.13), which indicated a reduction in the number of occupied sites. Site abandonment probabilities were greater at low elevations with warm temperatures. Other covariates, such as the presence of wildfire, nonnative brook trout, proximity to areas with many adults, and various stream habitat descriptors, were not associated with changes in probability of occupancy. Higher abandonment probabilities at low elevation for bull trout provide initial evidence validating the predictions made by bioclimatic models that bull trout populations will retreat to higher, cooler thermal refuges as water temperatures increase. The geographic breadth of these declines across the region is unknown but the approach of revisiting historical sites using an occupancy framework provides a useful template for additional assessments.

Effects of stocking-up freshwater food webs.

The establishment of exotic game fishes to enhance recreational fisheries through authorized and unauthorized stocking into freshwater systems is a global phenomenon. Stocked fishes are often top predators that either replace native top predators or increase the species richness of top predators. Many direct effects of stocking have been documented, but the ecosystem consequences are seldom quantified. New studies increasingly document how species and community shifts influence ecosystem processes. We discuss here how predator stocking might increase top-down effects, alter nutrient cycles and decrease links between aquatic and surrounding terrestrial ecosystems. As fisheries management moves beyond species-specific utilitarian objectives to incorporate ecosystem and conservation goals, ecologists must address how common management practices alter food-web structure and subsequent ecosystem-level effects.