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Caetano, Daniel S; Morlon, Hélène (Ed.)Abstract Ecological opportunity (EO) is an important catalyst for evolution. Whereas theory often centers around a lineage encountering a source of EO in isolation, in practice they experience numerous sources of opportunity, either concurrently or sequentially. Such multiplicity can obscure the macroevolutionary signature of EO. Here, we test the effects of elevation (a proxy of the “mountain effect”) and an array of functional innovations on the evolutionary history of plethodontid salamanders, a diverse and charismatic radiation of lungless amphibians. Functional innovations unlock access to novel microhabitats, ultimately enabling sub-lineages to occupy a diverse range of ecological niches, particularly in lowland areas where those niches are more abundant. Consistent with expanded ecological opportunity, such transitions to lower elevation result in rapid phenotypic evolution. At high elevation, by contrast, rates of phenotypic evolution and phenotypic disparity decline, reflecting a loss of phenotypically extreme ecological specialists. Transitions in elevation and the origin of innovations appear largely coincident among lungless salamanders, suggesting myriad sources of EO. The magnitude of the “mountain effect” on evolutionary rates (∼10-fold) is on par or greatly exceeds that of islands, lakes, and coral reefs on other iconic vertebrate radiations. Therefore, we find that elevation acts as a major ecological moderator and, in concert with functional innovations, shapes the ecological and phenotypic diversity of lungless salamanders.more » « less
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Thaker, Maria; Wolf, Jason (Ed.)Abstract Phenotypic expression is often constrained by functional conflicts between traits, and the resulting trade-offs impose limits on phenotypic and taxonomic diversity. However, the underlying mechanisms that maintain trade-offs or allow organisms to resolve them via phenotypic plasticity are often challenging to detect. The trade-off between gas exchange and water loss across respiratory surfaces represents a fundamental trade-off that constrains phenotypic diversity in terrestrial life. Here, we investigate plastic mechanisms that mitigate this trade-off in lungless salamanders that breathe exclusively across their skin. Our field and laboratory experiments identified plastic responses to environmental variation in water loss and oxygen uptake, and gene expression analyses identified putative pathways that regulate this trade-off. Although the trade-off was generally strong, its strength covaried with environmental conditions. At the molecular level, antagonistic pleiotropy in multiple biological pathways (e.g., vasoconstriction and upregulation of aerobic respiration) putatively produce the trade-off, while other pathways mitigate the trade-off by affecting a single trait (e.g., oxygen binding affinity, melanin synthesis). However, organisms are likely to encounter novel trade-offs in the process of bypassing another. Our study provides evidence that alternative pathways allow organisms to mitigate pleiotropic conflicts, which ultimately may allow greater phenotypic diversity and persistence in novel environments.more » « less
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Synopsis Wind can significantly influence heat and water exchange between organisms and their environment, yet microclimatic variation in wind is often overlooked in models forecasting the effects of environmental change on organismal performance. Accounting for the effects of wind may become even more critical given the anticipated changes in wind speed across the planet as climates continue to warm. In this study, we first assessed how wind speed varies across the planet and how wind speed may change under climate warming at macroclimatic scales. We also used microclimatic data to assess how wind speed changes temporally throughout the day and year as well as the relationship between wind speed, temperature, and standard deviation in each environmental variable using data from weather stations in North America. Finally, we used a suite of biophysical simulations to understand how wind speed (and its interactions with other environmental variables and organismal traits) affects the temperatures and rates of water loss that plants and animals experience at a microclimatic scale. We found substantial latitudinal variation in wind speed and the change in wind speed under climate change, demonstrating that temperate regions are predicted to experience simultaneous warming and reductions in wind speed. From the microclimatic data, we also found that wind speed is positively associated with temperature and temperature variability, indicating that the effects of wind speed may become more challenging to predict under future warming scenarios. The biophysical simulations demonstrated that convective and evaporative cooling from wind interacts strongly with organismal traits (such as body size, solar absorptance, and conductance) and the heating effects of solar radiation to shape heat and water fluxes in terrestrial plants and animals. In many cases, the effect of wind (or its interaction with other variables) was comparable to the effects of air temperature or solar radiation. Understanding these effects will be important for predicting the ecological impacts of climate change and for explaining clinal variation in traits that have evolved across a range of thermal environments.more » « less
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Synopsis Thermal gradient experiments are commonly used in studies of ectothermic organisms for a variety of scientific inquiries. Such gradient experiments, performed in the laboratory, are often used to infer the climatic preferences of animals in the absence of other variables. However, the ability to extrapolate laboratory results to the field is only as good as the accumulation of ecological data for that organism. When the variable quantified is interpreted as thermal “preference,” there are some assumptions that come with it, namely that the organism selects a particular preferred temperature by positive thermotaxis. Amphibians, as well as most ectotherms, tend to be thermoconformers, so conclusions from thermal gradient experiments carry different meanings than they do for organisms such as heliothermic ectotherms that maintain a narrow range of body temperatures in the lab and field. We tested whether and how the Eastern Red-backed Salamander (Plethodon cinereus) behaves when presented with a heterothermal gradient arena in comparison to a control (homothermal) arena. Salamanders in the control arena unambiguously moved toward either end of the arena, despite no variation in temperature being available. We found that salamanders did respond to a thermal gradient, but that their thermoregulatory behavior was limited to the avoidance of the hottest end of the gradient, and not a positive thermotaxis toward a specific temperature as assumed of a thermal “preference.” Our results encourage a broader consideration of how laboratory-measured behaviors relate to the predicted behaviors of organisms in natural settings, and a re-evaluation of the terminology used to describe movement behaviors in thermal gradients.more » « less
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ABSTRACT Mechanistic niche models are computational tools developed using biophysical principles to address grand challenges in ecology and evolution, such as the mechanisms that shape the fundamental niche and the adaptive significance of traits. Here, we review the empirical basis of mechanistic niche models in biophysical ecology, which are used to answer a broad array of questions in ecology, evolution and global change biology. We describe the experiments and observations that are frequently used to parameterize these models and how these empirical data are then incorporated into mechanistic niche models to predict performance, growth, survival and reproduction. We focus on the physiological, behavioral and morphological traits that are frequently measured and then integrated into these models. We also review the empirical approaches used to incorporate evolutionary processes, phenotypic plasticity and biotic interactions. We discuss the importance of validation experiments and observations in verifying underlying assumptions and complex processes. Despite the reliance of mechanistic niche models on biophysical theory, empirical data have and will continue to play an essential role in their development and implementation.more » « less
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Synopsis Terrestrial environments pose many challenges to organisms, but perhaps one of the greatest is the need to breathe while maintaining water balance. Breathing air requires thin, moist respiratory surfaces, and thus the conditions necessary for gas exchange are also responsible for high rates of water loss that lead to desiccation. Across the diversity of terrestrial life, water loss acts as a universal cost of gas exchange and thus imposes limits on respiration. Amphibians are known for being vulnerable to rapid desiccation, in part because they rely on thin, permeable skin for cutaneous respiration. Yet, we have a limited understanding of the relationship between water loss and gas exchange within and among amphibian species. In this study, we evaluated the hydric costs of respiration in amphibians using the transpiration ratio, which is defined as the ratio of water loss (mol H2O d−1) to gas uptake (mol O2 d−1). A high ratio suggests greater hydric costs relative to the amount of gas uptake. We compared the transpiration ratio of amphibians with that of other terrestrial organisms to determine whether amphibians had greater hydric costs of gas uptake relative to plants, insects, birds, and mammals. We also evaluated the effects of temperature, humidity, and body mass on the transpiration ratio both within and among amphibian species. We found that hydric costs of respiration in amphibians were two to four orders of magnitude higher than the hydric costs of plants, insects, birds, and mammals. We also discovered that larger amphibians had lower hydric costs than smaller amphibians, at both the species- and individual-level. Amphibians also reduced the hydric costs of respiration at warm temperatures, potentially reflecting adaptive strategies to avoid dehydration while also meeting the demands of higher metabolic rates. Our results suggest that cutaneous respiration is an inefficient mode of respiration that produces the highest hydric costs of respiration yet to be measured in terrestrial plants and animals. Yet, amphibians largely avoid these costs by selecting aquatic or moist environments, which may facilitate more independent evolution of water loss and gas exchange.more » « less
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Justin Boyles (Ed.)Abstract Hybridization between species affects biodiversity and population sustainability in numerous ways, many of which depend on the fitness of the hybrid relative to the parental species. Hybrids can exhibit fitter phenotypes compared to the parental lineages, and this ‘hybrid vigour’ can then lead to the extinction of one or both parental lines.In this study, we analysed the relationship between water loss and gas exchange to compare physiological performance among three tiger salamander genotypes—the native California tiger salamander (CTS), the invasive barred tiger salamanders (BTS) and CTS × BTS hybrids across multiple temperatures (13.5°C, 20.5°C and 23.5°C). We developed a new index of performance, the water‐gas exchange ratio (WGER), which we define as the ratio of gas exchange to evaporative water loss (μLVO2/μL H2O). The ratio describes the ability of an organism to support energetically costly activities with high levels of gas exchange while simultaneously limiting water loss to lower desiccation risk. We used flow through respirometry to measure the thermal sensitivity of metabolic rate and resistance to water loss of each salamander genotype to compare indices of physiological performance.We found that temperature had a significant effect on metabolic rate and resistance to water loss, with both traits increasing as temperatures warmed. Across genotypes, we found that hybrids have a higher WGER than the native CTS, owing to a higher metabolic rate despite having a lower resistance to water loss.These results provide a greater insight into the physiological mechanisms driving hybrid vigour and offer a potential explanation for the rapid spread of salamander hybrids. More broadly, our introduction of the WGER may allow for species‐ or lineage‐wide comparisons of physiological performance across changing environmental conditions, highlighting the insight that can be gleaned from multitrait analysis of organism performance. Read the freePlain Language Summaryfor this article on the Journal blog.more » « less
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Understanding how phenotypic plasticity is generated, whether through shared or divergent molecular mechanisms, is critical for predicting organismal responses to environmental change. Similar phenotypes can arise from different pathways, which may vary in costs, trade-offs, and consequences for performance. This study examined whether physiological plasticity in a woodland salamander (Plethodon metcalfi) was governed by common or distinct gene expression patterns across populations distributed along an elevational gradient. In a laboratory acclimation experiment, I measured plasticity in skin resistance to water loss and metabolic rate and used transcriptomic analyses to identify the underlying molecular mechanisms. Plasticity in skin resistance to water loss did not vary with elevation, yet the expression of molecular pathways associated with this plasticity differed depending on elevational origin. Low-elevation populations also tended to exhibit greater independent regulation of metabolic rate, despite the constraints imposed by the trade-off between metabolic rate and skin resistance. These findings reveal a distinct phenomenon: geographic divergence in plasticity mechanisms, where similar plastic phenotypes emerge from different molecular pathways. Despite being similar in magnitude, plasticity in some populations may be locally adapted through alternative mechanisms that differ in their costs and benefits, complicating our ability to predict responses to environmental change.more » « less
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