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Biology subjects

Riddell, E. A.

Publications and source records attributed to Riddell, E. A..

3 recordsLinked to original sources

Winter metabolic compensation endangers woodland salamanders under climate change

Understanding the mechanisms that shape species geographic distributions is essential for predicting responses to climate change, particularly under winter conditions, which are warming more rapidly than summer conditions in many temperate ecosystems. Woodland salamanders, which constitute many of the species in the global hotspot of salamander diversity located in the southern Appalachian Mountains of North America, are thought to cope with harsh winters through dormancy and metabolic suppression. We used a field-based experiment to investigate the winter physiology and energetics of a woodland salamander (Plethodon metcalfi). Despite showing histological signs of dormancy, salamanders exhibited higher metabolic rates during winter than the active season when measured at low temperatures associated with winter, consistent with metabolic compensation. High-elevation salamanders also exhibited elevated metabolic rates at cold temperatures compared to low-elevation salamanders, indicative of countergradient metabolic compensation. When integrated into a biophysical species distribution model, depletion of energy stores estimated from winter metabolic rates under current climates accurately predicted the geographic range limits of our focal species. Under future warming scenarios, incorporating winter physiology indicated that 77% of the species range would experience local extinction due to depletion of energy stores. These findings challenge assumptions about winter energetics, reveal metabolic limits on cold-season survival, and highlight metabolic demands during dormancy as a key constraint on responses to climate change.

ecology↗

Plastic mechanisms for unraveling a universal trade-off between water loss and respiration

The expression of phenotypes is often constrained by functional conflicts between traits, and the resulting trade-offs can impose limits on phenotypic and taxonomic diversity. However, organisms can circumvent trade-offs in specific environmental contexts through phenotypic plasticity, though the mechanisms that drive trade-offs or allow organisms to resolve trade-offs are often cryptic. The trade-off between water loss and gas exchange poses a fundamental challenge for terrestrial life because the capacity to absorb oxygen is limited by the risk of desiccation from water loss across respiratory surfaces. Here, we investigated the capacity to mitigate this trade-off in a lungless salamander that breathes exclusively across its skin. We measured water loss and oxygen uptake using respirometry in field- and laboratory-based studies to identify plastic responses to environmental variation, coupled with gene expression analyses to investigate biological pathways that regulate the trade-off. Though the trade-off between oxygen uptake and water loss was generally strong, we observed that its strength changed over time in the field and laboratory. At the molecular level, we found support for antagonistic pleiotropy in multiple pathways that simultaneously affect both physiological traits (e.g., via vasoconstriction and downregulation of aerobic respiration), and for mechanisms that mitigate the trade-off by affecting only one trait (e.g., oxygen binding affinity, melanin synthesis). As organisms disentangle such conflicts, however, alternative trade-offs are likely to arise. 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.

evolutionary biology↗

Environmentally robust cis-regulatory changes underlie rapid climatic adaptation

Changes in gene expression are proposed to play a major role in adaptive evolution. While it is known that gene expression is highly sensitive to the environment, very few studies have determined the influence of genetic and environmental effects on adaptive gene regulation in natural populations. Here, we utilize allele-specific expression to characterize cis and trans gene regulatory divergence in temperate and tropical house mice in two metabolic tissues under two thermal conditions. First, we show that gene expression divergence is pervasive between populations and across thermal conditions, with roughly 5-10% of genes exhibiting genotype-by-environment interactions. Second, we found that most expression divergence was due to cis-regulatory changes that were stable across temperatures. In contrast, patterns of expression plasticity were largely attributable to trans-effects, which showed greater sensitivity to temperature. Nonetheless, we discovered a small subset of temperature-dependent cis-regulatory changes, thereby identifying loci underlying expression plasticity. Finally, we performed scans for selection in wild house mice to identify genomic signatures of rapid adaptation. Genomic outliers were enriched in genes with evidence for cis-regulatory divergence. Notably, these genes were associated with phenotypes that affected body weight and metabolism, suggesting that cis-regulatory changes are a possible mechanism for adaptive body size evolution between populations. Our results show that gene expression plasticity, largely controlled in trans, may facilitate the colonization of new environments, but that evolved changes in gene expression are largely controlled in cis, illustrating the genetic and non-genetic mechanisms underlying the establishment of populations in new environments. Significance StatementGene expression variation is shaped by both genetic and environmental effects, yet these two factors are rarely considered together in the context of adaptive evolution. We studied environmental influences on gene regulatory evolution in temperate and tropical house mice in cold and warm laboratory environments. We discovered that genetic effects in the form of cis-regulatory divergence were pervasive and largely insensitive to the environment. Many of these genetic effects are under selection and are associated with genes that affect body size, suggesting cis-regulatory changes as a possible mechanism for adaptive body size evolution. We also discovered many trans-effects controlling expression plasticity, demonstrating the importance of both genetic and non-genetic changes associated with adaptation over short timescales (a few hundred generations).

evolutionary biology↗