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.

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.