1 Introduction

Gammarus, a highly diverse group of crustaceans, occupies an important ecological niche in freshwater and coastal ecosystems around the world. This group of organisms exhibits amazing environmental adaptability, and the study of their gene-environment interaction mechanism (G×E) provides a unique perspective for understanding species evolution. From streams and lakes to groundwaters and even deep-sea environments, gammarus maintains the material cycle of aquatic ecosystems by decomposing organic matter, and at the same time plays the role of an ecological sentinel as an important indicator species of environmental health. Its wide distribution and rich species composition are directly related to the stability and resilience of aquatic communities, and its sensitivity to environmental changes makes it a key model organism for studying the impact of human activities (Romanova et al., 2016; Jabłońska et al., 2020; Weigand et al., 2020; Benito et al., 2023).

Gene-environment interactions shape the evolutionary path of gammarus. The selective expression of specific mitochondrial and nuclear genes under environmental pressure drives the formation of local adaptive traits and promotes their rapid evolution in extreme environments (Fišer et al., 2015; Lan et al., 2017; Benito et al., 2023; Longo et al., 2024; Podwysocki et al., 2024). This dynamic interaction mechanism directly affects the genetic structure and long-term survival of populations.

In the context of current environmental upheavals, habitat fragmentation and climate change are reshaping natural selection pressures. These changes not only threaten the key genetic diversity that maintains species survival, but are also likely to change the original adaptive traits (Gaitán-Espitia and Hobday, 2020; Jabłońska et al., 2020; Pabijan et al., 2020; Weigand et al., 2020; Dewoody et al., 2021). Incorporating evolutionary mechanisms and G×E dynamics into conservation strategies can both ensure species survival and leave room for the evolution of new adaptive traits (Gaitán-Espitia and Hobday, 2020; Pabijan et al., 2020; Dewoody et al., 2021).

This study will integrate current knowledge about gene-environment interactions in amphipods, focusing on their implications for evolutionary processes and conservation management, summarize the ecological significance of amphipods, explore the mechanisms and consequences of gene-environment interactions in different habitats, and evaluate how these insights can guide conservation strategies under ongoing environmental change. This study provides a comprehensive framework for understanding and managing the diversity of amphipods in a rapidly changing world.

2 Ecological Diversity and Environmental Gradient Adaptation in Amphipods​

2.1 Habitat types and environmental variation factors​

Gammarus has a wide range of habitats: freshwater streams, rivers, and lakes are their homes; they can be found in brackish estuaries, groundwater systems, and cold springs; they can also be found in coastal areas with alternating high and low tides and in the depths of the ocean. From high mountain springs to the deep sea, from offshore shallows to offshore waters, the distribution span of gammarus is amazing. This not only demonstrates their super adaptability, but also highlights their key position in aquatic ecosystems (Altermatt et al., 2014; Lörz et al., 2021; Copilaș-Ciocianu and Sidorov, 2021; Momtazi and Saeedi, 2024; Ritter and Bourne, 2024).

The distribution pattern of gammarus is jointly shaped by a complex network of ecological factors. Water temperature fluctuations, salinity changes, dissolved oxygen concentration, pH levels, hydrodynamic characteristics, and the distribution of various pollutants or nutrients are all important influencing factors. Shallow water gammarus communities mainly respond to changes in temperature and chlorophyll concentration, while deep-sea populations show a complex response pattern of multi-factor synergy. Taking the North Sea and the Baltic Sea as examples, the significant difference in seawater salinity directly leads to obvious differentiation in ecological characteristics and genetic structure of gammarus in the two places. Changes in environmental gradients, especially continuous changes in dissolved oxygen content, pollutant concentrations, and water flow speeds, often trigger significant responses of gammarus in terms of distribution range, species diversity, and adaptive characteristics (Jourdan et al., 2019; Espinosa-Leal et al., 2021; Lörz et al., 2021; Geburzi et al., 2022; Cui et al., 2024; Momtazi and Saeedi, 2024).

2.2 Ecological adaptation types in amphipods​

Different body structures let amphipods adapt to many small habitats and do different jobs (like filtering food, digging holes, clinging to things, swimming, etc.). For example, Caprella have thin arms and legs. They often live on things like seaweed, holding on tightly to fit their life of clinging. Corophiidae are good at building tube-shaped nests and act like "engineering species." Gammarus are free-living bottom-dwellers, found in both fresh and salt water (Figure 1) (Ritter and Bourne, 2024). Amphipod groups can be mostly split into those that move around and those that stay in one place. Migratory species often use resources that change with the seasons or are in different places. Sedentary groups may adapt well to stable or extreme environments, like underground water or the deep sea (Altermatt et al., 2014; Copilaș-Ciocianu and Sidorov, 2021; Cui et al., 2024; Momtazi and Saeedi, 2024).

Figure 1 (A) Generalized body plan of a gammaridean amphipod, (B) Caprella equilibra, (C) family Corophiidae, and (D) Gammarus tigrinus (Adopted from Ritter and Bourne, 2024)

The life history strategies of gammarus exhibit amazing plasticity. Different populations may evolve very different survival strategies: some populations show rapid growth and high reproduction rates, while others tend to extend their lifespan and develop special reproductive mechanisms. This life history variation is closely related to environmental parameters, including ecological factors such as temperature fluctuation cycles, availability of food resources, and stability of habitat structure. Remarkably, even within a limited geographical scale, these environmental differences are sufficient to drive significant morphological differentiation among gammarus populations (Altermatt et al., 2014; Jourdan et al., 2019; Copilaș-Ciocianu and Sidorov, 2021).

Amphipods utilize a wide array of microhabitats, including under stones, within aquatic vegetation, in caves, and across vertical gradients in intertidal zones. Functional group composition and resource use strategies often shift with microhabitat, supporting ecosystem resilience and resource partitioning. This microhabitat specialization is a key factor in their ecological success and adaptive radiation (Scipione, 2013; Altermatt et al., 2014; Srinivas et al., 2020; Copilaș‐Ciocianu and Sidorov, 2021).

3 Research Progress on Gene–Environment Interactions in Amphipods

3.1 Environmental stress and gene expression responses in amphipods

Faced with extreme environmental pressures such as high water pressure, low temperature, and food shortage, gammarus have evolved a variety of physiological and molecular coping mechanisms. Taking the deep-sea gammarus Hirondellea gigas in the Mariana Trench as an example, genome studies have found that some of its genes have undergone functional changes - these genes are mostly related to energy metabolism, β-alanine synthesis, and genetic information processing. In addition, gene families related to low temperature adaptation and gene expression regulation have also expanded in number. These findings indicate that regulating gene function and expanding specific gene families are key ways for gammarus to adapt to extreme deep-sea environments (Lan et al., 2017). Other studies have shown that the microbiome on the surface of gammarus changes with parasitic pressure, which means that environmental stress (including interactions between organisms) may affect the gene expression and immune defense of gammarus (Koellsch et al., 2024).

3.2 G×E patterns revealed by genomic studies

Comparison of whole genome and mitochondrial gene studies confirmed that the living environment of gammarids has a significant impact on their genetic structure. The mitochondrial genome structure of surface and underground gammarids is significantly different, involving the gene arrangement form, order, and the intensity of selection pressure on genes related to energy metabolism. Surface species live in areas with large environmental fluctuations and high energy demand, and their energy genes involved in oxidative phosphorylation are subject to stronger directional selection pressure; underground species show stronger purifying selection, which is consistent with the ecological adaptation pattern of energy limitation in a stable environment (Benito et al., 2023). Deep-sea gammarids such as Halice and H. gigas are no exception. Their mitochondrial genome structure has significant variation and the amino acid composition of proteins is also unique. This further confirms the key role of gene-environment interaction (G×E) in the adaptation of the genome structure of gammarids (Lan et al., 2017; Li et al., 2019).

3.3 Role of epigenetic mechanisms in amphipod adaptation

Currently, direct studies on epigenetic mechanisms of gammarus (i.e., ways to regulate gene expression without changing the DNA sequence) are still relatively rare. However, gammarus can often quickly adjust their phenotype and function when the environment changes or after spreading to new areas, which suggests that epigenetic mechanisms may be involved. The invasive gammarus Dikerogammarus villosus is a typical example. They can present diverse body shapes and ecological traits in different environments. This adaptive flexibility may be due to epigenetic regulation that does not rely on gene mutations (Podwysocki et al., 2024). This suggests that it is necessary to further explore how epigenetics is involved in the gene-environment interaction and rapid adaptation process of gammarus.

4 Case Studies on G×E in Amphipods

4.1 G×E responses of freshwater amphipods to temperature variation

Comparative studies on mitochondrial genes have found that freshwater gammarus living on the surface and with large environmental fluctuations have genes related to energy metabolism, especially genes in the oxidative phosphorylation pathway, which are more susceptible to directional drive by natural selection. The high energy demand brought about by temperature fluctuations has become the key to promoting genetic adaptation of these gammarus, helping them to cope with variable temperature environments. In contrast, gammarus living in underground waters, where the temperature is stable and the environment is cold, their genes are under stronger conservative selection pressure. There is no need to adapt to temperature changes quickly, making their genetic level more stable (Benito et al., 2023).

4.2 Gene–environment interactions in salinity tolerance of marine amphipods

The study of the invasive species Dikerogammarus villosus revealed the profound impact of salinity gradient on phenotypic plasticity. Individuals living in high-salt environments showed more developed predatory organs, and this morphological differentiation directly confirmed the regulatory role of gene-environment interaction (G×E) in salinity adaptation. It is worth noting that the evolutionary history of differences between populations will significantly change the pattern and degree of G×E response, indicating that the formation of salt tolerance traits originates from the dynamic interaction between genetic background and environmental factors (Podwysocki et al., 2024).

4.3 G×E studies on adaptive evolution of amphipods in polluted environments

The study of the genetic mechanism of pollution adaptation of Dikerogammarus villosus is still blank, but the study of parasite interactions provides important inspiration. Environmental stress such as parasitic infection can significantly change the structure of the microbial community on the body surface, and this change may regulate the gene expression network through host-microbe interaction. Specifically, the composition of the surface microbiota of parasite-infected hook shrimp is systematically different from that of healthy individuals, and this difference may reshape the adaptive evolutionary trajectory of the host through pathways such as immune regulation. These findings suggest that pollutants may be similar to parasite stress, activating specific G×E response patterns through the synergistic mechanism of gene expression reprogramming and microbiome reconstruction (Koellsch et al., 2024).

5 Evolutionary Insights from G×E Studies in Amphipods

5.1 Adaptive evolution driven by gene–environment interactions

The study of Gammarus revealed a complex mechanism by which environmental heterogeneity and historical events synergistically drive speciation. The population of Gammarus roeselii in the Balkan Peninsula exhibited a typical cryptic species phenomenon, and at least 13 genetically differentiated populations were found to have highly similar morphological characteristics. The origin and differentiation of these populations were significantly associated with Neogene geological changes and the evolution of the hydrological pattern in the Pleistocene, fully demonstrating the dual role of ancient and modern environmental changes in shaping genetic diversity and promoting speciation through G×E interactions (Grabowski et al., 2017). Similarly, the Hyalella gammarus population in the ancient lakes of the Andes showed rapid morphological differentiation and convergent evolution after appearing in new habitats, providing an ideal model for studying microscale evolutionary processes (Zapelloni et al., 2021).

Genomic analysis further confirmed that the populations of gammarids showed significant G×E-related genetic variation under different habitat conditions (such as temperature and salinity gradients). The mitochondrial genome of the deep-sea gammarid Halice sp. exhibited unique structural rearrangements and amino acid variation patterns, which are likely to be adaptive responses to the extreme deep-sea environment (Li et al., 2019). Together, these findings suggest that G×E interactions can not only drive the generation of new adaptive traits, but also reshape the genetic architecture and phenotypic characteristics of species under the combined effects of ancient and modern environmental pressures (Grabowski et al., 2017; Li et al., 2019; Zapelloni et al., 2021).

5.2 Niche conservatism and expansion revealed by G×E studies

G×E studies of gammarids reveal the balancing mechanism of species maintaining niche conservation and achieving niche expansion. In the Ampithoe marcuzzii group, the synergistic effect of environmental factors and geographic isolation led to significant differentiation between continental and island populations. Environmental differences and geographic distances not only limit gene exchange, but also record the genetic imprint of historical expansion. Although island populations have limited dispersal capacity, they can achieve niche expansion with the help of floating objects and changes in ocean currents; however, continental populations are more sensitive to local climate change due to limited gene flow and tend to maintain niche stability (Iwasa-Arai et al., 2024). The niche migration phenomenon of the rosenbergii shrimp between lake and river habitats in the Balkans also confirms this law. Ancient lakes, as climate refuges, not only maintain niche conservatism, but also provide the possibility for niche expansion, which profoundly explains the dynamic relationship between gene × niche interaction and niche evolution (Grabowski et al., 2017).

6 Applied Value of G×E Research in Amphipod Conservation and Management

6.1 Species conservation and risk assessment

Gene-environment interaction (G×E) analysis can effectively identify cryptic species and intraspecific genetic variation, providing a scientific basis for conservation decisions. Modern molecular techniques such as DNA barcoding can accurately identify cryptic species and their population structure characteristics, and assist in the delineation of priority conservation areas. Research data specifically point out that populations with unique genetic composition need to be protected, especially rare genotypes distributed in upstream waters. In-depth analysis of intraspecific genetic differences can help assess population connectivity, resilience and environmental sensitivity, thereby supporting the formulation of differentiated conservation policies (Weigand et al., 2020; Huang et al., 2023).

6.2 Environmental monitoring and ecosystem health evaluation

As a sensitive indicator species of environmental change, hook shrimp exhibit significant G×E response characteristics. Studies have found that populations with similar genetic backgrounds have obvious differentiation in physiological responses to micropollutants and pesticides in different regions. By tracking changes in its gene expression profile and physiological indicators, early warning of ecosystem degradation can be provided, and high-risk areas of environmental pollution or habitat destruction can be accurately identified. The population dynamics of gammarus are significantly positively correlated with aquatic plant diversity, making it an ideal "umbrella species" for assessing the health of the overall ecosystem (Švara et al., 2021; Larson et al., 2022).

6.3 Ecological restoration and adaptive management applications

G×E research provides key theoretical support for ecological restoration. Clarifying the dependence of gammarus on specific habitats and its diffusion restrictions is of guiding significance for the formulation of scientific ex situ conservation plans. Ex situ experiments have confirmed that the effect of population reconstruction depends not only on the matching degree of the genetic background of the introduced site and the source population, but also on the precise regulation of key environmental factors. The habitat suitability model constructed by integrating genetic and environmental parameters can significantly improve the accuracy of restoration site selection and the success rate of population reconstruction (Weigand et al., 2020; Fitzpatrick et al., 2024).

7 Challenges and Future Trends in Amphipod G×E Research

7.1 Technical and methodological challenges

In recent years, research on the interaction between genes and the environment (G×E) in gammarus has increased, but it is still limited by some technical and methodological bottlenecks, making it difficult to expand to a deeper and broader dimension. The lack of high-quality genetic information resources is a prominent problem. Although some common gammarus species have transcriptome data (i.e., gene expression information), most species lack complete reference genomes, which directly limits the identification of functional genes and regulatory sequences involved in environmental response (Reid et al., 2021). In addition, it is technically difficult to simulate real environmental stresses (such as salinity changes, temperature fluctuations, and pollutant exposure) under experimental conditions. Many G×E effects are context-dependent and often require long-term or multi-generation exposure to appear. Short-term experiments naturally cannot accurately capture these changes.

Another key problem is telling apart traits that change because of the environment (plastic responses) from those that are passed down through genes (heritable G×E interactions). Amphipods often change their traits based on the environment. Some traits that were thought to come from genetic adaptation might actually come from changes in gene activity passed through generations or shifts in the tiny organisms living on them. Also, many G×E studies use small numbers of samples and don't test many populations, which makes their results less statistically strong. Simple linear models might not be enough to find complex interactions between many genes or non-linear effects from the environment (Hoffmann and Rieseberg, 2008).

7.2 Interdisciplinary integration and technological developments

The future of G×E research in gammarus cannot be separated from the drive of emerging technologies and the deep integration of interdisciplinary studies. The introduction of multi-omics approaches - covering genomics, transcriptomics, epigenomics and metabolomics - provides powerful tools for multi-level analysis of G×E mechanisms. For example, studies have discovered stress pathways related to metal stress and heat stress through transcriptome analysis. The emergence of emerging environmental sensing technologies and high-throughput trait measurement platforms has made it possible to track environmental changes and physiological responses of gammarus in real time under natural or semi-natural conditions (Boyd et al., 2022).

Although gene editing technologies such as CRISPR/Cas9 have not yet been popularized in gammarus research, their potential in functional gene verification and G×E mechanism testing cannot be underestimated. At the same time, the development of landscape genomics and spatialized population models can reveal selection patterns under different environmental conditions and help understand the adaptability of gammarus to the local environment and the mechanism of coping with climate change (Funk et al., 2012; Wang et al., 2013). Only by integrating these data into an eco-evolutionary framework can a model be constructed to predict the response of populations under environmental pressure.

7.3 Future research recommendations

To promote the development of G×E research on gammarus, efforts can be made from the following aspects. First, it is urgent to build a more complete genetic database of gammarus, giving priority to representative species with significant differences in ecological functions. Establishing a reference genome at the chromosome level and collecting genetic data from multiple populations can not only improve the precision of G×E analysis, but also help to identify key genes related to environmental adaptation. Second, a unified G×E research design standard should be formulated to make the results of different research systems and different stress factors comparable. This includes standardized gammarus stress experimental protocols, standardized trait measurement methods, and unified statistical analysis processes.

Third, G×E research on amphipods should be combined with demographic and ecological models. This will help assess how genetic variation affects evolution and conservation. Such models can identify traits that are being selected for and predict how populations will change as the environment changes. Fourth, working together across disciplines—between molecular biologists, ecotoxicologists, ecologists, and conservation workers—is needed to deal with the many factors involved in G×E responses in real environments. Finally, we stress the need to focus on traits related to survival, like how many offspring are produced, and behavior. These traits directly connect G×E interactions to how ecosystems work and why conservation matters.

8 Concluding Remarks

The latest research has found that the genetic and physiological functions of hook shrimps have changed significantly in the process of adapting to diverse and even extreme environments. Studies on gene expression (transcriptomics) and mitochondrial genome (mitochondrial genomics) show that survival in deep sea, underground and cold environments depends on the selection of specific genes - these genes are closely related to energy metabolism, the expansion of specific gene families, and the unique variation of mitochondrial genome structure. The results of the study highlight that gene-environment interactions (G×E) play a key role in driving the evolution of hook shrimp genes and forming functional diversity. The type of habitat and the environmental pressure jointly shape the evolutionary trajectory of gene expression regulation and genome structure. Not only that, the interaction between hook shrimps and parasites and the changes in the surface microbiome highlight the complex connotation of the G×E mechanism in the life history of hook shrimps.​

Knowing about G×E in amphipods is key for guessing how they will react to environmental changes and for planning ways to protect them. Amphipods' ability to adapt to extreme conditions shows how tough they are ecologically and why they are good as bioindicators. Learning about genetic differences, ways they adapt, and how their tiny organism communities change can help with risk checks, habitat management, and protecting populations that are at risk or found only in certain areas. This is especially important as habitats get damaged and the climate changes.​

Future research should bring together advanced studies of genes, active genes, and tiny organism communities to better understand how G×E works in amphipods. Doing more studies that include more species, homes, and environmental differences will improve our knowledge of adaptive evolution and help with conservation work. Focusing on working across different science areas and watching over long periods will be necessary to create flexible management plans. These plans will help amphipod populations survive and keep their ecological roles in changing environments.

Acknowledgments

Members also thank the laboratory team for their support and cooperation.

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.

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