Outbreeding reduces survival during metamorphosis in a headwater stream salamander.

Assessing direct fitness effects of individual genetic diversity is challenging due to the intensive and long-term data needed to quantify survival and reproduction in the wild. But resolving these effects is necessary to determine how inbreeding and outbreeding influence eco-evolutionary processes. We used 8 years of capture-recapture data and single nucleotide polymorphism genotypes for 1906 individuals to test for effects of individual heterozygosity on stage-specific survival probabilities in the salamander Gyrinophilus porphyriticus. The life cycle of G. porphyriticus includes an aquatic larval stage followed by metamorphosis into a semi-aquatic adult stage. In our study populations, the larval stage lasts 6-10 years, metamorphosis takes several months, and lifespan can reach 20 years. Previous studies showed that metamorphosis is a sensitive life stage, leading us to predict that fitness effects of individual heterozygosity would occur during metamorphosis. Consistent with this prediction, monthly probability of survival during metamorphosis declined with multi-locus heterozygosity (MLH), from 0.38 at the lowest MLH (0.10) to 0.06 at the highest MLH (0.38), a reduction of 84%. Body condition of larvae also declined significantly with increasing MLH. These relationships were consistent in the three study streams. With evidence of localised inbreeding within streams, these results suggest that outbreeding disrupts adaptations in pre-metamorphic and metamorphic individuals to environmental gradients along streams, adding to evidence that headwater streams are hotspots of microgeographic adaptation. Our results also underscore the importance of incorporating life history in analyses of the fitness effects of individual genetic diversity and suggest that metamorphosis and similar discrete life stage transitions may be critical periods of viability selection.

Stage-Specific Demographic Effects of Hydrologic Variation in a Stream Salamander.

AbstractWe lack a strong understanding of how organisms with complex life histories respond to climate variation. Many stream-associated species have multistage life histories that are likely to influence the demographic consequences of floods and droughts. However, tracking stage-specific demographic responses requires high-resolution, long-term data that are rare. We used 8 years of capture-recapture data for the headwater stream salamander Gyrinophilus porphyriticus to quantify the effects of flooding and drying magnitude on stage-specific vital rates and population growth. Drying reduced larval recruitment but increased the probability of metamorphosis (i.e., adult recruitment). Flooding reduced adult recruitment but had no effect on larval recruitment. Larval and adult survival declined with flooding but were unaffected by drying. Annual population growth rates (λ) declined with flooding and drying. Lambda also declined over the study period (2012-2021), although mean λ was 1.0 over this period. Our results indicate that G. porphyriticus populations are resilient to hydrologic variation because of compensatory effects on recruitment of larvae versus adults (i.e., reproduction vs. metamorphosis). Complex life cycles may enable this resilience to climate variation by creating opportunities for compensatory demographic responses across stages. However, more frequent and intense hydrologic variation in the latter half of this study contributed to a decline in λ over time, suggesting that increasing environmental variability poses a threat even when demographic compensation occurs.

Individual growth rates and size at metamorphosis increase with watershed area in a stream salamander.

A fundamental goal of ecology is to understand how the physical environment influences intraspecific variability in life history and, consequently, fitness. In streams, discharge and associated habitat conditions change along a continuum from intermittency to permanence: Headwater streams typically have smaller watersheds and are thus more prone to drying than higher-order streams with larger watersheds and more consistent discharge. However, few empirical studies have assessed life history and associated population responses to this continuum in aquatic organisms. We tested the prediction that individual growth, rate of development, and population growth increase with watershed area in the long-lived stream salamander Gyrinophilus porphyriticus, where we use watershed area as a proxy for hydrologic intermittence. To address this hypothesis, we used 8 years of mark-recapture data from 53 reaches across 10 headwater streams in New Hampshire, USA. Individual growth rates and mean size at metamorphosis increased with watershed area for watersheds from 0.12 to 1.66 km2 . Population growth rates increased with watershed area; however, this result was not statistically significant at our sample size. Mean age of metamorphosis did not vary across watershed areas. Lower individual growth rates and smaller sizes at metamorphosis likely contributed to reduced lifetime fecundity and population growth in reaches with the smallest watershed areas and highest vulnerability to drought. These responses suggest that as droughts increase due to climate change, headwater specialists in hydrologically intermittent environments will experience a reduction in fitness due to smaller body sizes or other growth-related mechanisms.

Source-sink dynamics within a complex life history.

Source-sink patch dynamics occur when movement from sources stabilizes sinks by compensating for low local vital rates. The mechanisms underlying source-sink dynamics may be complicated in species that undergo transitions between discrete life stages, particularly when stages have overlapping habitat requirements and similar movement abilities. In these species, for example, the demographic effects of movement by one stage may augment or offset the effects of movement by another stage. We used a stream salamander system to investigate patch dynamics within this form of complex life history. Specifically, we tested the hypothesis that the salamander Gyrinophilus porphyriticus experiences source-sink dynamics in riffles and pools, the dominant geomorphic patch types in headwater streams. We estimated stage-specific survival probabilities in riffles and pools and stage-specific movement probabilities between the two patch types using 8 years of capture-recapture data on 4491 individuals, including premetamorphic larvae and postmetamorphic adults. We then incorporated survival and movement probabilities into a stage-structured, two-patch model to determine the demographic interactions between riffles and pools. Monthly survival probabilities of both stages were higher in pools than in riffles. Larvae were more likely to move from riffles to pools, but adults were more likely to move from pools to riffles, despite experiencing much lower survival in riffles. In simulations, eliminating interpatch movements by both stages indicated that riffles are sinks that rely on immigration from pools for stability. Allowing only larvae to move stabilized both patch types, but allowing only adults to move destabilized pools due to the demographic cost of adult emigration. These results indicated that larval movement not only stabilizes riffles, but also offsets the destabilizing effects of maladaptive adult movement. Similar patch dynamics may emerge in any structured population in which movement and local vital rates differ by age, size, or stage. Addressing these forms of internal demographic structure in patch dynamics analyses will help to refine and advance general understanding of spatial ecology.

Environmentally Associated Variation in Dispersal Distance Affects Inbreeding Risk in a Stream Salamander.

AbstractAvoiding inbreeding is considered a key driver of dispersal evolution, and dispersal distances should be especially important in mediating inbreeding risk because the likelihood of mating with relatives decreases with dispersal distance. However, a lack of direct data on dispersal distances has limited empirical tests of this prediction, particularly in the context of the multiple selective forces that can influence dispersal. Using the headwater stream salamander Gyrinophilus porphyriticus, we tested whether spatial variation in environmental conditions leads to differences in dispersal distances, resulting in spatial variation in the effect of dispersal on inbreeding risk. Using capture-recapture and population genomic data from five streams, we found that dispersal distances were greater in downstream reaches than upstream reaches. Inbreeding risk trended lower for dispersers than nondispersers in downstream reaches but not in upstream reaches. Furthermore, stream reaches did not differ in spatial patterns of individual relatedness, indicating that variation in inbreeding risk was in fact due to differences in dispersal distances. These results demonstrate that environmentally associated variation in dispersal distances can cause the inbreeding consequences of dispersal to vary at fine spatial scales. They also show that selective pressures other than inbreeding avoidance maintain phenotypic variation in dispersal, underscoring the importance of addressing alternative hypotheses in dispersal research.

Differences in Corticosterone Release Rates of Larval Spring Salamanders (Gyrinophilus porphyriticus) in Response to Native Fish Presence.

Invasive fish predators are an important factor causing amphibian declines and may have direct and indirect effects on amphibian survival. For example, early non-lethal exposure to these stressors may reduce survival in later life stages, especially in biphasic species. In amphibians, the glucocorticoid hormone corticosterone is released by the hypothalamo-pituitary-interrenal axis (HPI), as an adaptive physiological response to environmental stressors. The corticosterone response (baseline and response to acute stressors) is highly flexible and context dependent, and this variation can allow individuals to alter their phenotype and behavior with environmental changes, ultimately increasing survival. We sampled larvae of the spring salamander (Gyrinophilus porphyriticus) from two streams that each contained predatory brook trout (Slavelinus fontinalis) in the lower reaches and no predatory brook trout in the upper reaches. We measured baseline and stress-induced corticosterone release rates of larvae from the lower and upper reaches using a non-invasive water-borne hormone assay. We hypothesized that corticosterone release rates would differ between larvae from fish-present reaches and larvae from fish-free reaches. We found that baseline and stressor-induced corticosterone release rates were downregulated in larvae from reaches with fish predators. These results indicate that individuals from reaches with predatory trout are responding to fish predators by downregulating corticosterone while maintaining an active HPI axis. This may allow larvae more time to grow before metamorphosing, while also allowing them to physiologically respond to novel stressors. However, prolonged downregulation of corticosterone release rates can impact growth in post-metamorphic individuals.

Sex-related differences in aging rate are associated with sex chromosome system in amphibians.

Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture-recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the "unguarded X/Z effect") or repeat-rich Y/W chromosome (the "toxic Y/W effect") could accelerate aging in the heterogametic sex in some vertebrate clades.

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.

Metamorphosis in an Era of Increasing Climate Variability.

Most animals have complex life cycles including metamorphosis or other discrete life stage transitions, during which individuals may be particularly vulnerable to environmental stressors. With climate change, individuals will be exposed to increasing thermal and hydrologic variability during metamorphosis, which may affect survival and performance through physiological, behavioral, and ecological mechanisms. Furthermore, because metamorphosis entails changes in traits and vital rates, it is likely to play an important role in how populations respond to increasing climate variability. To identify mechanisms underlying population responses and associated trait and life history evolution, we need new approaches to estimating changes in individual traits and performance throughout metamorphosis, and we need to integrate metamorphosis as an explicit life stage in analytical models.

Long-term survival probability, not current habitat quality, predicts dispersal distance in a stream salamander.

Dispersal evolves as an adaptive mechanism to optimize individual fitness across the landscape. Specifically, dispersal represents a mechanism to escape fitness costs resulting from changes in environmental conditions. Decades of empirical work suggest that individuals use local habitat cues to make movement decisions, but theory predicts that dispersal can also evolve as a fixed trait, independent of local conditions, in environments characterized by a history of stochastic spatiotemporal variation. Until now, however, both conditional and fixed models of dispersal evolution have primarily been evaluated using emigration data (stay vs. leave), and not dispersal distances: a more comprehensive measure of dispersal. Our goal was to test whether conditional or fixed models of dispersal evolution predict variation in dispersal distance in the stream salamander Gyrinophilus porphyriticus. We quantified variation in habitat conditions using measures of salamander performance from 4 yr of spatially explicit, capture-mark-recapture (CMR) data across three headwater streams in the Hubbard Brook Experimental Forest in central New Hampshire, USA. We used body condition as an index of local habitat quality that individuals may use to make dispersal decisions, and survival probability estimated from multistate CMR models as an index of mortality risk resulting from the long-term history of environmental variation. We found that dispersal distances increased with declining survival probability, indicating that salamanders disperse further in risky environments. Dispersal distances were unrelated to spatial variation in body condition, suggesting that salamanders do not base dispersal distance decisions on local habitat quality. Our study provides the first empirical support for fixed models of dispersal evolution, which predict that dispersal evolves in response to a history of spatiotemporal environmental variation, rather than as a conditional response to current habitat conditions. More broadly, this study underscores the value of assessing alternative scales of environmental variation to gain a more complete and balanced understanding of dispersal evolution.

A distance-performance trade-off in the phenotypic basis of dispersal.

Across taxa, individuals vary in how far they disperse, with most individuals staying close to their origin and fewer dispersing long distances. Costs associated with dispersal (e.g., energy, risk) are widely believed to trade off with benefits (e.g., reduced competition, increased reproductive success) to influence dispersal propensity. However, this framework has not been applied to understand variation in dispersal distance, which is instead generally attributed to extrinsic environmental factors. We alternatively hypothesized that variation in dispersal distances results from trade-offs associated with other aspects of locomotor performance. We tested this hypothesis in the stream salamander Gyrinophilus porphyriticus and found that salamanders that dispersed farther in the field had longer forelimbs but swam at slower velocities under experimental conditions. The reduced swimming performance of long-distance dispersers likely results from drag imposed by longer forelimbs. Longer forelimbs may facilitate moving longer distances, but the proximate costs associated with reduced swimming performance may help to explain the rarity of long-distance dispersal. The historical focus on environmental drivers of dispersal distances misses the importance of individual traits and associated trade-offs among traits affecting locomotion.

Hydrologic variability contributes to reduced survival through metamorphosis in a stream salamander.

Changes in the amount, intensity, and timing of precipitation are increasing hydrologic variability in many regions, but we have little understanding of how these changes are affecting freshwater species. Stream-breeding amphibians-a diverse group in North America-may be particularly sensitive to hydrologic variability during aquatic larval and metamorphic stages. Here, we tested the prediction that hydrologic variability in streams decreases survival through metamorphosis in the salamander Gyrinophilus porphyriticus, reducing recruitment to the adult stage. Using a 20-y dataset from Merrill Brook, a stream in northern New Hampshire, we show that abundance of G. porphyriticus adults has declined by ∼50% since 1999, but there has been no trend in larval abundance. We then tested whether hydrologic variability during summers influences survival through metamorphosis, using capture-mark-recapture data from Merrill Brook (1999 to 2004) and from 4 streams in the Hubbard Brook Experimental Forest (2012 to 2014), also in New Hampshire. At both sites, survival through metamorphosis declined with increasing variability of stream discharge. These results suggest that hydrologic variability reduces the demographic resilience and adaptive capacity of G. porphyriticus populations by decreasing recruitment of breeding adults. They also provide insight on how increasing hydrologic variability is affecting freshwater species, and on the broader effects of environmental variability on species with vulnerable metamorphic stages.

Spatial capture-recapture reveals age- and sex-specific survival and movement in stream amphibians.

Life-history information sets the foundation for our understanding of ecology and conservation requirements. For many species, this information is lacking even for basic demographic rates such as survival and movement. When survival and movement estimates are available, they are often derived from mixed demographic groups and do not consider differences among life stages or sexes, which is critical, because life stages and sexes often contribute differentially to population dynamics. We used hierarchical models informed with spatial capture-mark-recapture data of Ascaphus montanus (Rocky Mountain tailed frog) in five streams and A. truei (coastal tailed frog) in one stream to estimate variation in survival and movement by sex and age, represented by size. By incorporating survival and movement into a single model, we were able to estimate both parameters with limited bias. Annual survival was similar between sexes of A. montanus [females = 0.885 (95% CI 0.614-1), males = 0.901 (0.657-1)], but was slightly higher for female A. truei [0.836 (0.560-0.993)] than for males [0.664 (0.354-0.962)]. Survival of A. montanus peaked at mid-age, suggesting that lower survival of young and actuarial senescence may influence population demographics. Our models suggest that younger A. montanus moved farther than older individuals, and that females moved farther than males in both species. Our results provide uncommon insight into age- and sex-specific rates of survival and movement that are crucial elements of life-history strategies and are important for modeling population growth and prescribing conservation actions.

Mercury bioaccumulation in temperate forest food webs associated with headwater streams.

The soils and food webs associated with mid to high elevation, forested, headwater streams in northeastern North America are potential hotspots for mercury (Hg) methylation and bioaccumulation, but are not well studied. Our goals were to quantify total Hg (THg) and methyl Hg (MeHg) concentrations in soils and terrestrial food webs associated with headwater streams of northern hardwood forests to identify predictors of small-scale spatial variation in Hg bioaccumulation. We sampled soil characteristics that promote Hg methylation including pH, sulfur and calcium content, and organic matter. To assess spatial variation, we sampled at high (~700 m asl) and mid elevations (~500 m asl), both adjacent to (<1 m) and away from (>75 m) three replicate headwater streams in each of two watersheds of the White Mountains region, New Hampshire, USA. Soils of these forested watersheds differed significantly in pH and the content of calcium, sulfur, organic matter and THg. Conditions for methylation were more favorable in the upland forest sites compared to streamside sites. Significant bioaccumulation of THg occurred in all measured components of the food web, including insects, spiders, salamanders, and birds. Trophic position, as determined by δ15N, was the best predictor of both THg and MeHg bioaccumulation across the sampled taxa and was also a better predictor than spatial location. However, the degree of bioaccumulation at which MeHg significantly affects animal behavior, reproduction or survival is unknown for most taxa in terrestrial habitats, particularly for invertebrates. These findings show that Hg methylation and bioaccumulation is not limited to areas traditionally classified as wetlands or to areas with exceptionally high THg inputs, but that it is a widespread and important phenomenon in the moist deciduous forests of eastern North America.

Matching habitat choice and plasticity contribute to phenotype-environment covariation in a stream salamander.

Populations optimize the match of phenotype to environment by localized natural selection, adaptive phenotypic plasticity, and habitat choice. Habitat choice may also be achieved by several mechanisms, including matching habitat choice, where individuals distribute themselves based on self-assessment of the phenotype-environment match. Matching habitat choice is a relatively untested concept, but one that could advance our understanding of the interplay of movement ecology and intraspecific phenotypic variation. Morphology of the salamander Gyrinophilus porphyriticus differs in riffles and pools, the dominant habitats in headwater streams where this species occurs. Specifically, individuals found in riffles have shorter limbs than those found in pools. Here, we used 4 yr of spatially explicit capture-mark-recapture data from three streams to test the contributions of phenotypic plasticity and matching habitat choice to this phenotype-environment covariation. We quantified morphological variation in G. porphyriticus with size-corrected principal component (PC) scores and assessed phenotype-environment match based on the difference between habitats in these PC scores. We found that both phenotypic plasticity and matching habitat choice contribute to phenotype-environment covariation in G. porphyriticus. The phenotypes of individuals that switched habitats (i.e., riffle→pool, pool→riffle) changed to become better matched to the recipient habitat, indicating a plastic response to local habitat conditions. Consistent with matching habitat choice, individuals were also more likely to switch habitats if their initial phenotype was a better match to the alternative habitat, independent of subsequent changes in morphology due to plasticity. Realized performance, survival adjusted for the likelihood of remaining in each habitat, was higher in individuals with phenotypes matched to each habitat than in those with mismatched phenotypes, but performance was generally lower in riffles than pools, suggesting that other factors influence the use of riffles. Our results underscore the value of considering how matching habitat choice interacts with other mechanisms that allow organisms to maximize performance when faced with environmental heterogeneity. More broadly, our study shows that it is important to account for movement in any study of the causes or consequences of intraspecific trait variation, a challenge that may require novel research approaches and experimental designs.

Evolutionary Community Ecology: Time to Think Outside the (Taxonomic) Box.

Ecologists and evolutionary biologists have long been interested in the role of interspecific competition in the diversification of clades. These studies often focus on a single taxonomic group, making the implicit assumption that important competitive interactions occur only between closely related taxa, despite abundant documentation of intense competition between species that are distantly related. Specifically, this assumption ignores convergence of distantly related competitors on limiting niche axes and thus may miss cryptic effects of distantly related competitors on the evolution of focal clades. For example, distantly related competitors may act as important drivers of niche conservatism within clades, a pattern commonly ascribed to evolutionary constraints or the abiotic environment. Here we propose an alternative model of how niche similarity evolves when the functional traits of interest are mediated by unrelated phenotypic traits, as is often the case for distantly related competitors. This model represents an important conceptual step towards a more accurate, taxonomically inclusive understanding of the role that competition plays in the micro- and macroevolution of interacting species.

Legacy introductions and climatic variation explain spatiotemporal patterns of invasive hybridization in a native trout.

Hybridization between invasive and native species, a significant threat to worldwide biodiversity, is predicted to increase due to climate-induced expansions of invasive species. Long-term research and monitoring are crucial for understanding the ecological and evolutionary processes that modulate the effects of invasive species. Using a large, multidecade genetics dataset (N = 582 sites, 12,878 individuals) with high-resolution climate predictions and extensive stocking records, we evaluate the spatiotemporal dynamics of hybridization between native cutthroat trout and invasive rainbow trout, the world's most widely introduced invasive fish, across the Northern Rocky Mountains of the United States. Historical effects of stocking and contemporary patterns of climatic variation were strongly related to the spread of hybridization across space and time. The probability of occurrence, extent of, and temporal changes in hybridization increased at sites in close proximity to historical stocking locations with greater rainbow trout propagule pressure, warmer water temperatures, and lower spring precipitation. Although locations with warmer water temperatures were more prone to hybridization, cold sites were not protected from invasion; 58% of hybridized sites had cold mean summer water temperatures (<11°C). Despite cessation of stocking over 40 years ago, hybridization increased over time at half (50%) of the locations with long-term data, the vast majority of which (74%) were initially nonhybridized, emphasizing the chronic, negative impacts of human-mediated hybridization. These results show that effects of climate change on biodiversity must be analyzed in the context of historical human impacts that set ecological and evolutionary trajectories.

Population Genetics and Demography Unite Ecology and Evolution.

The interplay of ecology and evolution has been a rich area of research for decades. A surge of interest in this area was catalyzed by the observation that evolution by natural selection can operate at the same contemporary timescales as ecological dynamics. Specifically, recent eco-evolutionary research focuses on how rapid adaptation influences ecology, and vice versa. Evolution by non-adaptive forces also occurs quickly, with ecological consequences, but understanding the full scope of ecology-evolution (eco-evo) interactions requires explicitly addressing population-level processes - genetic and demographic. We show the strong ecological effects of non-adaptive evolutionary forces and, more broadly, the value of population-level research for gaining a mechanistic understanding of eco-evo interactions. The breadth of eco-evolutionary research should expand to incorporate the breadth of evolution itself.