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.

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.

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.