Species' ecological preferences are often deduced from habitat characteristics thought to represent more or less optimal conditions for physiological functioning. Evolution has led to stenotopic and eurytopic species, the former having decreased niche breadths and lower tolerances to environmental variability. Species inhabiting freshwater springs are often described as being stenotopic specialists, adapted to the stable thermal conditions found in these habitats. Whether due to past local adaptation these species have evolved or have lost intra‐generational adaptive mechanisms to cope with increasing thermal variability has, to our knowledge, never been investigated. By studying how the proteome of a stenotopic species changes as a result of increasing temperatures, we investigate if the absence or attenuation of molecular mechanisms is indicative of local adaptation to freshwater springs. An understanding of compensatory mechanisms is especially relevant as spring specialists will experience thermal conditions beyond their physiological limits due to climate change. In this study, the stenotopic species Crunoecia irrorata (Trichoptera: Lepidostomatidae, Curtis 1834) was acclimated to 10, 15 and 20°C for 168 hr. We constructed a homology‐based database and via liquid chromatography‐tandem mass spectrometry (LC‐MS/MS)‐based shotgun proteomics identified 1,358 proteins. Differentially abundant proteins and protein norms of reaction revealed candidate proteins and molecular mechanisms facilitating compensatory responses such as trehalose metabolism, tracheal system alteration and heat‐shock protein regulation. A species‐specific understanding of compensatory physiologies challenges the characterization of species as having narrow tolerances to environmental variability if that characterization is based on occurrences and habitat characteristics alone.

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Our ability to predict and assess how environmental changes such as pollution and climate change affect components of the Earth’s biome is of paramount importance. This need positioned the fields of ecotoxicology and stress ecology at the center of environmental monitoring efforts. Advances in these interdisciplinary fields depend not only on conceptual leaps but also on technological advances and data integration. High-throughput “omics” technologies enabled the measurement of molecular changes at virtually all levels of an organism’s biological organization and thus continue to influence how the impacts of stressors are understood. This bibliometric review describes literature trends (2000–2020) that indicate that more different stressors than species are studied each year but that only a few stressors have been studied in more than two phyla. At the same time, the molecular responses of a diverse set of non-model species have been investigated, but cross-species comparisons are still rare. While transcriptomics studies dominated until 2016, a shift towards proteomics and multiomics studies is apparent. There is now a wealth of data at functional omics levels from many phylogenetically diverse species. This review, therefore, addresses the question of how to integrate omics information across species.

Deducing impacts of environmental change on species and the populations they form in nature is an important goal in contemporary ecology. Achieving this goal is hampered by our limited understanding of the influence of naturally occurring environmental variation on the molecular systems of ecologically relevant species, as the pathways underlying fitness-affecting plastic responses have primarily been studied in model organisms and under controlled laboratory conditions. Here, to test the hypothesis that proteome variation systematically relates to variation in abiotic conditions, we establish such relationships by profiling the proteomes of 24 natural populations of the spring-dwelling caddisfly Crunoecia irrorata. We identified protein networks whose abundances correlated with environmental (abiotic) gradients such as in situ pH, oxygen- and nitrate concentrations but also climatic data such as past thermal minima and temperature seasonality. Our analyses suggest that variations in abiotic conditions induce discrete proteome responses such as the differential abundance of proteins associated with cytoskeletal function, heat-shock proteins and proteins related to post-translational modification. Identifying these drivers of proteome divergence characterizes molecular “noise”, and positions it as a background against which molecular signatures of species’ adaptive responses to stressful conditions can be identified.

Species' acclimation capacities and their ability to maintain molecular homeostasis outside of ideal temperature ranges will partly predict their success following climate-change induced thermal regime shifts. Theory predicts that ectothermic organisms from thermally stable environments have muted plasticities, and that these species may be particularly vulnerable to temperature increase. Whether such species retained or lost acclimation capacities remains largely unknown. We studied proteome changes in the planarian Crenobia alpina, a prominent member of cold-stable alpine habitats that is considered to be cold-adapted stenotherm. We found that the species’ CTmax is above its experienced habitat temperatures and that different populations exhibit differential CTmax acclimation capacities, whereby an alpine population showed reduced plasticity. In a separate experiment, we acclimated C. alpina individuals from the alpine population to 8, 11, 14, or 17°C over the course of 168 h and compared a comprehensively annotated species-specific proteome. Network analyses of 3399 proteins and protein set enrichment show that while the species’ proteome is overall stable across these temperatures, protein sets functioning in oxidative stress response, mitochondria, protein synthesis and turnover are lower abundant following warm acclimation. Proteins associated with an unfolded protein response, ciliogenesis, tissue damage repair, development, and the innate immune system were higher abundant following warm acclimation. Our findings suggest that this species has not suffered DNA decay (e.g., loss of heat-shock proteins) during evolution in a cold-stable environment and retained plasticity in response to elevated temperatures, challenging the notion that stable environments necessarily result in muted plasticity.