1 Introduction

Gammarus species, a group of freshwater crustaceans, play a crucial role in aquatic ecosystems as they contribute significantly to the decomposition of organic matter and serve as a vital food source for various fish and bird species. These organisms are often used as sentinel species in ecotoxicological studies due to their sensitivity to environmental changes and pollutants (Cribiu et al., 2018). Their ecological relevance is underscored by their widespread presence in natural stream communities, where they help maintain the balance of aquatic ecosystems.

Gammarus species are increasingly exposed to various environmental stressors, including chemical pollutants and habitat alterations. These stressors can significantly impact their physiological and reproductive processes. For instance, exposure to endocrine-disrupting chemicals (EDCs) such as cadmium and other xenobiotics has been shown to alter sperm quality and protein expression in Gammarus fossarum, indicating a disruption in reproductive health (Trapp et al., 2015). Additionally, changes in water temperature and food availability can lead to modifications in genomic cytosine methylation levels, which are potential markers of environmental stress (Cribiu et al., 2018).

Genomic studies provide valuable insights into the adaptive mechanisms of Gammarus species in response to environmental changes. By examining epigenetic marks such as cytosine methylation, researchers can assess how these organisms modulate their genetic expression in response to stressors (Cribiu et al., 2018). Proteomic analyses further reveal the biological impacts of toxic exposure, highlighting changes in protein expression that are crucial for understanding the resilience and vulnerability of Gammarus to environmental pressures (Trapp et al., 2015).

This study aims to synthesize current knowledge on the environmental genomics of Gammarus species, focusing on their responses to habitat changes and stressors. By integrating findings from genomic and proteomic studies, the study seeks to elucidate the molecular and physiological adaptations of these organisms, to enhance the understanding of Gammarus as sentinel species and to inform conservation strategies that mitigate the impacts of environmental stressors on aquatic ecosystems.

2 Environmental Stressors Impacting Gammarus Populations

2.1 Pollution and contaminant accumulation in aquatic ecosystems

Pollution, particularly from heavy metals like cadmium, significantly impacts Gammarus populations. Exposure to cadmium results in epigenetic changes, such as hypomethylation followed by hypermethylation, which can serve as biomarkers for environmental stress in these organisms (Cribiu et al., 2018). Additionally, pollution from anthropogenic sources, including changes in river morphology and the introduction of alien species, affects the genetic diversity and adaptability of Gammarus pulex, highlighting the species' sensitivity to environmental contaminants (Švara et al., 2019).

2.2 Temperature variations and thermal stress adaptation

Temperature changes are another critical stressor for Gammarus species. Studies have shown that increased water temperatures lead to hypermethylation in Gammarus fossarum, indicating a stress response at the genomic level (Cribiu et al., 2018). This adaptation mechanism is crucial for survival as it allows Gammarus to cope with thermal stress, which is increasingly relevant in the context of global climate change.

2.3 Salinity and osmotic stress in freshwater and brackish habitats

Gammarus species have historically adapted to shifts between saline and freshwater environments, which has driven diversification. The transition from saline to freshwater habitats in the Eocene led to increased diversification rates in Gammarus, suggesting that salinity changes are a significant evolutionary driver (Hou et al., 2011). Furthermore, the invasion of Gammarus tigrinus into both brackish and freshwater habitats demonstrates the species' ability to adapt to varying salinity levels, although this can lead to reduced genetic diversity due to bottlenecks (Kelly et al., 2006).

2.4 Oxygen availability and responses to hypoxia

Oxygen availability is a crucial factor affecting Gammarus populations, particularly in habitats prone to hypoxia. While specific studies on Gammarus’ response to hypoxia are limited, the general sensitivity of freshwater organisms to oxygen levels suggests that hypoxia could significantly impact their survival and distribution. The genetic structure of Gammarus fossarum, for instance, is influenced by environmental factors, including oxygen availability, which affects gene flow and population connectivity (Weiss and Leese, 2016).

2.5 Habitat fragmentation and its effects on genetic diversity

Habitat fragmentation poses a significant threat to the genetic diversity of Gammarus populations. In human-impacted landscapes, Gammarus fossarum populations exhibit strong genetic differentiation due to isolation, which is exacerbated by anthropogenic barriers such as water reservoirs. This isolation can lead to genetic drift and reduced genetic diversity, making populations more vulnerable to environmental changes and less adaptable to new stressors. The diversification of Gammarus pecos in isolated desert springs further illustrates how habitat fragmentation can drive speciation and genetic differentiation (Adams et al., 2018).

3 Genomic Approaches to Studying Gammarus Adaptation

3.1 Population genomics and genetic diversity assessments

Population genomics is a powerful tool for assessing genetic diversity and understanding the adaptive potential of Gammarus species. Studies have utilized microsatellite markers to analyze the genetic structure of Gammarus populations, revealing significant genetic differentiation even over small geographic scales. For instance, research on Gammarus pulex has shown that novel microsatellite markers can effectively characterize genetic diversity and population structure, highlighting the impact of anthropogenic changes on genetic patterns (Švara et al., 2019). Similarly, investigations into Gammarus fossarum have demonstrated that genetic drift and historical colonization events significantly influence population structure, with limited gene flow due to habitat fragmentation and human impacts (Weiss and Leese, 2016). These findings underscore the importance of fine-scale genetic studies to identify barriers to gene flow and maintain genetic diversity in freshwater ecosystems.

3.2 Transcriptomic responses to environmental stressors

Transcriptomic analyses provide insights into how Gammarus species respond to environmental stressors at the molecular level. For example, RNA-Seq studies on Gammarus minus have identified differentially expressed genes between cave and surface populations, indicating adaptive responses to subterranean environments (Carlini and Fong, 2017). This research found that a significant number of transcripts were upregulated in cave populations, suggesting positive selection on genes associated with cave adaptation. Additionally, transcriptomic studies have revealed that environmental stressors such as temperature and chemical exposure can lead to changes in gene expression, which may serve as biomarkers for environmental stress (Cribiu et al., 2018). These transcriptomic responses highlight the complex interplay between environmental factors and gene expression, providing a deeper understanding of the mechanisms underlying Gammarus adaptation to changing habitats.

3.3 Epigenetics and phenotypic plasticity in Gammarus

Epigenetic mechanisms, such as DNA methylation, play a crucial role in the phenotypic plasticity and adaptation of Gammarus species to environmental changes. Research on Gammarus fossarum has shown that environmental stressors, including temperature fluctuations and chemical exposure, can alter global cytosine methylation levels, indicating that epigenetic modifications are responsive to environmental conditions. These changes in methylation patterns may serve as potential markers for environmental stress and contribute to the phenotypic plasticity observed in Gammarus populations. The study of epigenetic responses in non-model organisms like Gammarus is still in its infancy, but it holds promise for understanding how these species adapt to rapidly changing environments.

3.4 Functional genomics for identifying key adaptive genes

Functional genomics approaches, such as sequencing and analyzing specific genes, are essential for identifying key adaptive genes in Gammarus species. Studies have utilized phylogenetic analyses and gene sequencing to explore the evolutionary history and diversification of Gammarus, revealing how habitat shifts have influenced genetic adaptations (Hou et al., 2011). For instance, the transition from saline to freshwater habitats has been linked to increased diversification rates in Gammarus, driven by ecological opportunities and changes in environmental conditions (Adams et al., 2018). Additionally, research on mitochondrial genomes has identified genetic adaptations to extreme environments, such as high altitudes, in Gammarus species, highlighting the role of positive selection in shaping genetic diversity (Sun et al., 2020). These functional genomics studies provide valuable insights into the genetic basis of adaptation and the evolutionary processes driving diversification in Gammarus.

4 Molecular Pathways Involved in Environmental Responses

4.1 Stress Response Genes and Heat Shock Proteins

Heat shock proteins (Hsps) are crucial in the stress response of organisms, acting as molecular chaperones that help maintain protein homeostasis under stressful conditions. These proteins are highly conserved across species and are upregulated in response to various stressors, including heat, toxins, and environmental changes (Rhee et al., 2009; Chen et al., 2018). The Hsp70 family, in particular, is extensively studied for its role in thermotolerance and its response to xenobiotic exposure. In the intertidal copepod Tigriopus japonicus, Hsp70 expression is significantly induced by heat and exposure to trace metals and endocrine-disrupting chemicals, suggesting a protective role against environmental stressors (Rhee et al., 2009). Similarly, in the reef coral Montastraea franksi, Hsp70 and Hsp90 are upregulated in response to heavy metals and oil dispersants, indicating a general cellular stress response (Venn et al., 2009).

The expression of Hsps is not only a response to immediate stress but also plays a role in long-term adaptation and evolutionary fitness. Advances in genomic technologies have revealed the complexity of the heat shock response, showing that it involves multiple biological processes and systems. The regulatory variation and epigenetic changes in Hsp genes highlight their evolutionary significance as capacitors that can influence the evolution of other genes and ecological interactions. Moreover, in aquatic organisms, Hsps are involved in immune responses, assisting in the defense against pathogens and environmental stressors.

4.2 Detoxification pathways and xenobiotic metabolism

Detoxification pathways are essential for organisms to manage and mitigate the effects of xenobiotics, which include both natural and anthropogenic compounds. The aryl hydrocarbon receptor (AhR) signaling pathway is a key player in the detoxification response, regulating the expression of enzymes involved in metabolizing xenobiotics. In the clam Ruditapes philippinarum, the AhR pathway is activated by polycyclic aromatic hydrocarbons (PAHs), leading to the induction of detoxification enzymes and antioxidant defenses (Wang et al., 2020). This pathway involves interactions with other signaling pathways, such as the Nrf2-Keap1 and MAPK pathways, to enhance the organism's ability to cope with environmental stressors.

In insects, the transcriptional regulation of detoxification genes is mediated by various signaling pathways, including nuclear receptors and GPCRs. These pathways facilitate the upregulation of detoxification enzymes in response to xenobiotic exposure, contributing to metabolic resistance and adaptation to environmental changes. The expression of detoxification-related genes is also influenced by polymorphisms in transcription factor binding motifs, which can affect the organism's adaptive processes (Amezian et al., 2021). Additionally, the expression of heat shock proteins, such as Hsp70 and Hsp90, is linked to detoxification processes, as seen in the clam Ruditapes philippinarum, where these proteins are involved in the metabolic detoxification of benzo (a) pyrene (Liu et al., 2015).

4.3 Immune system adaptations to pathogenic and environmental stress

The immune system of aquatic organisms is intricately linked to their ability to respond to environmental stressors and pathogens. Heat shock proteins play a significant role in modulating immune responses, acting as chaperones that assist in protein folding and assembly, which is crucial during stress conditions (Jeyachandran et al., 2023). In aquatic organisms like fish and shrimp, Hsps are upregulated in response to pathogen invasion, enhancing both specific and non-specific immune responses. This upregulation can be induced through non-traumatic methods, such as the administration of Hsp stimulants, which help reduce physical stress and improve health outcomes in aquaculture practices.

Moreover, the immune response to environmental stress is also mediated by detoxification pathways. The AhR signaling pathway, for instance, not only regulates detoxification enzymes but also interacts with immune-related pathways to bolster the organism's defense mechanisms (Wang et al., 2020). This interaction is crucial for maintaining homeostasis and ensuring survival in environments with fluctuating levels of pollutants and pathogens. The integration of detoxification and immune responses highlights the complex interplay between different molecular pathways in adapting to environmental challenges.

4.4 Osmoregulation and ion transport mechanisms

Osmoregulation and ion transport are vital processes that enable organisms to maintain cellular homeostasis in varying environmental conditions. While the provided data does not directly address osmoregulation and ion transport mechanisms, it is known that these processes are often linked to stress response pathways. Heat shock proteins, for example, can influence ion transport by stabilizing proteins involved in these processes, thereby aiding in the maintenance of cellular homeostasis under stress (Jeyachandran et al., 2023).

In aquatic environments, organisms must constantly adjust their osmoregulatory mechanisms to cope with changes in salinity and other environmental factors. The expression of stress response genes, including Hsps, can be indicative of the organism's ability to manage these changes. Although specific studies on osmoregulation in Gammarus are not detailed in the provided data, the general principles of stress response and detoxification pathways are likely to play a role in supporting osmoregulatory functions in these organisms.

5 Case Study: Genomic Adaptation of Gammarus pulex to Pollution Stress

5.1 Background on Gammarus pulex and its ecological role

Gammarus pulex, a freshwater amphipod, plays a crucial role in aquatic ecosystems as a detritivore, contributing to the breakdown of organic matter and serving as a key food source for various predators. This species is widely distributed in European streams and rivers, where it is often used as a bioindicator due to its sensitivity to environmental changes and pollutants (Shahid et al., 2018). The ecological significance of G. pulex is underscored by its involvement in nutrient cycling and its impact on the structure of aquatic communities. Its presence and health can reflect the overall condition of the aquatic environment, making it an important species for monitoring ecosystem health (Yardy and Callaghan, 2020).

5.2 Genetic and epigenetic responses to heavy metal and pesticide contamination

Gammarus pulex exhibits notable genetic and epigenetic adaptations when exposed to pollutants such as heavy metals and pesticides. Studies have shown that populations exposed to low levels of pesticides develop increased tolerance, which is likely a result of genetic adaptation and possibly epigenetic modifications. For instance, exposure to neonicotinoid insecticides has led to a significant increase in tolerance levels in G. pulex populations, suggesting a rapid evolutionary response to chemical stressors (Siddique et al., 2020). Additionally, proteomic analyses have identified changes in protein expression related to metabolic pathways, indicating biochemical adaptations to pollutants like PCBs and cadmium (Leroy et al., 2010). These adaptations highlight the complex interplay between genetic and environmental factors in shaping the resilience of G. pulex to pollution stress.

5.3 Transcriptomic changes in polluted vs. clean water environments

The transcriptomic profile of Gammarus pulex varies significantly between polluted and clean water environments. In polluted habitats, G. pulex exhibits altered expression of genes involved in stress response, detoxification, and metabolic processes (Cogne et al., 2019). For example, exposure to heavy metals and pesticides has been associated with changes in the expression of genes related to oxidative stress and energy metabolism, reflecting the organism's efforts to mitigate the toxic effects of these contaminants (Tatar and Türkmenoğlu, 2020). Henry et al. (2017) studied the effects of ammonia stress and heat stress on the Gammarus genus and measured the response of Hsp70 (heat shock protein 70).

5.4 Implications for conservation and ecotoxicology

The genomic and transcriptomic adaptations of Gammarus pulex to pollution stress have significant implications for conservation and ecotoxicology. Understanding these adaptive responses can inform risk assessments and the development of strategies to mitigate the impacts of pollutants on aquatic ecosystems (Cold and Forbes, 2004). The ability of G. pulex to adapt to low levels of contaminants suggests that current regulatory thresholds may need to be re-evaluated to ensure the protection of sensitive species and ecosystem functions (Siddique et al., 2020). Furthermore, the study of G. pulex as a model organism can enhance our understanding of the broader ecological consequences of pollution and guide conservation efforts aimed at preserving biodiversity and ecosystem services in freshwater environments (Yardy and Callaghan, 2020).

6 Comparative Genomics Across Gammarus Species

6.1 Genetic adaptation patterns in different Gammarus species

Gammarus species exhibit diverse genetic adaptation patterns in response to varying environmental conditions. For instance, Gammarus pulex has been studied for its ability to adapt to anthropogenic environmental changes, such as pollution and habitat alterations. The development of novel microsatellite markers has facilitated the analysis of genetic differentiation among populations, revealing distinct genetic lineages within the species (Švara et al., 2019). Similarly, Gammarus fossarum shows significant genetic structure influenced by historical colonization events and anthropogenic impacts, highlighting the role of genetic drift in isolated populations (Weiss and Leese, 2016). These studies underscore the importance of genetic tools in understanding the adaptive strategies of Gammarus species in response to environmental stressors.

In addition to microsatellite analysis, proteomic studies have provided insights into the physiological adaptations of Gammarus species. For example, Gammarus pulex populations exposed to cadmium contamination exhibit proteome divergence, with proteins involved in stress responses being more abundant in contaminated sites (Cogne et al., 2019). This suggests that Gammarus species can undergo significant physiological changes to cope with environmental stress, further illustrating the complexity of their genetic adaptation mechanisms.

6.2 Convergent vs. divergent evolutionary strategies in habitat adaptation

Gammarus species demonstrate both convergent and divergent evolutionary strategies in adapting to their habitats. The study of Gammarus lacustris and Gammarus pisinnus reveals that these species have developed distinct mitochondrial adaptations to cope with the extreme conditions of the Qinghai-Tibet Plateau. While G. lacustris exhibits strong purifying selection, G. pisinnus shows signs of directional and relaxed selection, indicating divergent evolutionary strategies despite their geographical proximity (Sun et al., 2020). This divergence is likely driven by the unique ecological niches and environmental pressures faced by each species.

Conversely, the habitat selection and distribution patterns of Gammarus species in different regions suggest convergent evolutionary strategies. In the Baltic Sea, for example, Gammarus species exhibit habitat compression and coexistence, with selection pressures leading to similar adaptations across species. This convergence is likely a result of shared environmental gradients and the need to avoid interspecific competition, highlighting the complex interplay between evolutionary strategies and habitat adaptation.

6.3 Insights from model organisms and related crustaceans

Research on model organisms and related crustaceans provides valuable insights into the evolutionary dynamics of Gammarus species. The transcriptomic analysis of Gammarus minus, a model organism for studying subterranean adaptation, reveals positive selection on cave-downregulated transcripts, suggesting that genetic variation is shaped by the unique environmental conditions of cave habitats (Carlini and Fong, 2017). This study highlights the potential for using transcriptomic data to uncover the genetic basis of adaptation in Gammarus species.

Furthermore, the diversification patterns of Gammarus species in response to historical habitat shifts offer insights into their evolutionary trajectories. The transition from saline to freshwater habitats during the Eocene led to increased diversification rates in Gammarus, driven by ecological opportunities and changes in the Tethys and landmass (Hou et al., 2011). These findings demonstrate the influence of historical and environmental factors on the evolutionary pathways of Gammarus species, providing a broader context for understanding their genomic adaptations.

7 Conservation and Management Implications

7.1 Using genomic data to monitor Gammarus population health

Genomic data can be instrumental in monitoring the health of Gammarus populations by identifying genetic variations that indicate local adaptation and potential maladaptation to environmental changes. The concept of genomic offset, which assesses the degree of maladaptation by comparing genomic and environmental data, can be particularly useful in this context (Rellstab et al., 2021; Gain et al., 2023). By understanding the genetic structure and variability within Gammarus populations, conservationists can better predict how these populations might respond to environmental stressors such as pollution or habitat fragmentation.

7.2 Habitat restoration strategies based on genetic insights

Genetic insights can guide habitat restoration strategies by identifying key environmental factors that influence genetic variation and adaptation. For instance, landscape genomics can reveal how genetic variations are associated with specific environmental gradients, which can inform the selection of sites for restoration efforts (Feng and Du, 2022). Additionally, understanding the genetic structure of Gammarus populations can help identify suitable donor populations for conservation translocations, ensuring that genetic diversity is maintained and that translocated populations are well-adapted to their new environments.

7.3 Predicting future Gammarus adaptation under climate change

Predicting how Gammarus populations will adapt to climate change involves understanding the genetic basis of their responses to environmental changes. Genomic data can help model the potential for local adaptation and identify regions where populations may be at risk due to climate change (Fitzpatrick and Keller, 2015; Chen et al., 2021). By mapping the geographic distribution of genetic variations, researchers can predict areas where Gammarus populations might face challenges in adapting to future climates, allowing for proactive conservation measures (Rodríguez-Correa et al., 2018).

7.4 Policy recommendations for freshwater and estuarine conservation

Policy recommendations for the conservation of freshwater and estuarine ecosystems should incorporate genomic data to enhance the effectiveness of conservation strategies. This includes using genomic insights to inform habitat restoration, conservation translocations, and the management of genetic diversity within populations (Carlini and Fong, 2017). Policymakers should also consider the potential impacts of climate change on genetic diversity and adaptation, ensuring that conservation efforts are resilient to future environmental changes (Weiss and Leese, 2016).

Acknowledgments

The author extends sincere thanks to two anonymous peer reviewers for their feedback on the manuscript.

Conflict of Interest Disclosure

The author affirms that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

References

Adams N., Inoue K., Seidel R., Lang B., and Berg D., 2018, Isolation drives increased diversification rates in freshwater amphipods, Molecular Phylogenetics and Evolution, 127: 746-757.

https://doi.org/10.1016/j.ympev.2018.06.022

Carlini D., and Fong D., 2017, The transcriptomes of cave and surface populations of Gammarus minus (Crustacea: Amphipoda) provide evidence for positive selection on cave downregulated transcripts, PLoS ONE, 12(10): e0186173.

https://doi.org/10.1371/journal.pone.0186173

Chen B., Feder M., and Kang L., 2018, Evolution of heat-shock protein expression underlying adaptive responses to environmental stress, Molecular Ecology, 27: 3040-3054.

https://doi.org/10.1111/mec.14769

Chen Z., Grossfurthner L., Loxterman J., Masingale J., Richardson B., Seaborn T., Smith B., Waits L., and Narum S., 2021, Applying genomics in assisted migration under climate change: Framework, empirical applications, and case studies, Evolutionary Applications, 15: 3-21.

https://doi.org/10.1111/eva.13335

Cogne Y., Almunia C., Gouveia D., Pible O., François A., Degli-Esposti D., Geffard O., Armengaud J., and Chaumot A., 2019, Comparative proteomics in the wild: Accounting for intrapopulation variability improves describing proteome response in a Gammarus pulex field population exposed to cadmium, Aquatic Toxicology, 214: 105244.

https://doi.org/10.1016/j.aquatox.2019.105244

Cold A., and Forbes V., 2004, Consequences of a short pulse of pesticide exposure for survival and reproduction of Gammarus pulex, Aquatic Toxicology, 67(3): 287-299.

https://doi.org/10.1016/j.aquatox.2004.01.015

Cribiu P., Chaumot A., Geffard O., Ravanat J., Bastide T., Delorme N., Quéau H., Caillat S., Devaux A., and Bony S., 2018, Natural variability and modulation by environmental stressors of global genomic cytosine methylation levels in a freshwater crustacean, Gammarus fossarum, Aquatic Toxicology, 205: 11-18.

https://doi.org/10.1016/j.aquatox.2018.09.015

Feng L., and Du F., 2022, Landscape genomics in tree conservation under a changing environment, Frontiers in Plant Science, 13: 822217.

https://doi.org/10.3389/fpls.2022.822217

Fitzpatrick M., and Keller S., 2015, Ecological genomics meets community-level modelling of biodiversity: Mapping the genomic landscape of current and future environmental adaptation, Ecology Letters, 18(1): 1-16.

https://doi.org/10.1111/ele.12376

Gain C., Rhoné B., Cubry P., Salazar I., Forbes F., Vigouroux Y., Jay F., and François O., 2023, A quantitative theory for genomic offset statistics, Molecular Biology and Evolution, 40(6): msad140.

https://doi.org/10.1093/molbev/msad140

Henry Y., Piscart C., Charles S., and Colinet H., 2017, Combined effect of temperature and ammonia on molecular response and survival of the freshwater crustacean Gammarus pulex, Ecotoxicology and Environmental Safety, 137: 42-48.

https://doi.org/10.1016/j.ecoenv.2016.11.011

Hou Z., Šket B., Fišer C., and Li S., 2011, Eocene habitat shift from saline to freshwater promoted Tethyan amphipod diversification, Proceedings of the National Academy of Sciences of the United States of America, 108: 14533-14538.

https://doi.org/10.1073/pnas.1104636108

Jeyachandran S., Chellapandian H., Park K., and Kwak I., 2023, A review on the involvement of heat shock proteins (extrinsic chaperones) in response to stress conditions in aquatic organisms, Antioxidants, 12(7): 1444.

https://doi.org/10.3390/antiox12071444

Kelly D., Muirhead J., Heath D., and MacIsaac H., 2006, Contrasting patterns in genetic diversity following multiple invasions of fresh and brackish waters, Molecular Ecology, 15(12): 3641-3653.

https://doi.org/10.1111/j.1365-294X.2006.03012.x

Leroy D., Haubruge E., Pauw E., Thomé J., and Francis F., 2010, Development of ecotoxicoproteomics on the freshwater amphipod Gammarus pulex: Identification of PCB biomarkers in glycolysis and glutamate pathways, Ecotoxicology and Environmental Safety, 73(3): 343-352.

https://doi.org/10.1016/j.ecoenv.2009.11.006

Liu T., Pan L., Cai Y., and Miao J., 2015, Molecular cloning and sequence analysis of heat shock proteins 70 (HSP70) and 90 (HSP90) and their expression analysis when exposed to benzo(a)pyrene in the clam Ruditapes philippinarum, Gene, 555(2): 108-118.

https://doi.org/10.1016/j.gene.2014.10.051

Martins K., Gugger P., Llanderal-Mendoza J., González-Rodríguez A., Fitz-Gibbon S., Zhao J., Rodríguez-Correa H., Oyama K., and Sork V., 2018, Landscape genomics provides evidence of climate-associated genetic variation in Mexican populations of Quercus rugosa, Evolutionary Applications, 11: 1842-1858.

https://doi.org/10.1111/eva.12684

Rellstab C., Dauphin B., and Expósito-Alonso M., 2021, Prospects and limitations of genomic offset in conservation management, Evolutionary Applications, 14: 1202-1212.

https://doi.org/10.1111/eva.13205

Rhee J., Raisuddin S., Lee K., Seo J., Ki J., Kim I., Park H., and Lee J., 2009, Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants, Comparative Biochemistry and Physiology, Part C, Toxicology & Pharmacology, 149(1): 104-112.

https://doi.org/10.1016/j.cbpc.2008.07.009

Shahid N., Becker J., Krauss M., Brack W., and Liess M., 2018, Adaptation of Gammarus pulex to agricultural insecticide contamination in streams, The Science of the Total Environment, 621: 479-485.

https://doi.org/10.1016/j.scitotenv.2017.11.220

Siddique A., Liess M., Shahid N., and Becker J., 2020, Insecticides in agricultural streams exert pressure for adaptation but impair performance in Gammarus pulex at regulatory acceptable concentrations, The Science of the Total Environment, 722: 137750.

https://doi.org/10.1016/j.scitotenv.2020.137750

Sun S., Wu Y., Ge X., Jakovlić I., Zhu J., Mahboob S., Al-Ghanim K., Al-Misned F., and Fu H., 2020, Disentangling the interplay of positive and negative selection forces that shaped mitochondrial genomes of Gammarus pisinnus and Gammarus lacustris, Royal Society Open Science, 7(1): 190669.

https://doi.org/10.1098/rsos.190669

Švara V., Norf H., Luckenbach T., Brack W., and Michalski S., 2019, Isolation and characterization of eleven novel microsatellite markers for fine-scale population genetic analyses of Gammarus pulex (Crustacea: Amphipoda), Molecular Biology Reports, 46: 6609-6615.

https://doi.org/10.1007/s11033-019-05077-y

Tatar Ş., and Türkmenoğlu Y., 2020, Investigation of antioxidant responses in Gammarus pulex exposed to bisphenol A, Environmental Science and Pollution Research, 27: 12237-12241.

https://doi.org/10.1007/s11356-020-07834-0

Trapp J., Armengaud J., Pible O., Gaillard J., Abbaci K., Habtoul Y., Chaumot A., and Geffard O., 2015, Proteomic investigation of male Gammarus fossarum, a freshwater crustacean, in response to endocrine disruptors, Journal of Proteome Research, 14(1): 292-303.

https://doi.org/10.1021/pr500984z

Venn A., Quinn J., Jones R., and Bodnar A., 2009, P-glycoprotein (multi-xenobiotic resistance) and heat shock protein gene expression in the reef coral Montastraea franksi in response to environmental toxicants, Aquatic Toxicology, 93(4): 188-195.

https://doi.org/10.1016/j.aquatox.2009.05.003

Wang H., Pan L., Zhang X., Ji R., Si L., and Cao Y., 2020, The molecular mechanism of AhR-ARNT-XREs signaling pathway in the detoxification response induced by polycyclic aromatic hydrocarbons (PAHs) in clam Ruditapes philippinarum, Environmental Research, 183: 109165.

https://doi.org/10.1016/j.envres.2020.109165

Weiss M., and Leese F., 2016, Widely distributed and regionally isolated! Drivers of genetic structure in Gammarus fossarum in a human-impacted landscape, BMC Evolutionary Biology, 16(1): 153.

https://doi.org/10.1186/s12862-016-0723-z

Yardy L., and Callaghan A., 2020, What the fluff is this?—Gammarus pulex prefer food sources without plastic microfibers, The Science of the Total Environment, 715: 136815.

https://doi.org/10.1016/j.scitotenv.2020.136815