The Evolutionary Ecology of Animals Inhabiting Hydrogen Sulfide–Rich Environments

Abstract

Hydrogen sulfide (H2S) is a respiratory toxicant that creates extreme environments tolerated by few organisms. H2S is also produced endogenously by metazoans and plays a role in cell signaling. The mechanisms of H2S toxicity and its physiological functions serve as a basis to discuss the multifarious strategies that allow animals to survive in H2S-rich environments. Despite their toxicity, H2S-rich environments also provide ecological opportunities, and complex selective regimes of covarying abiotic and biotic factors drive trait evolution in organisms inhabiting H2S-rich environments. Furthermore, adaptation to H2S-rich environments can drive speciation, giving rise to biodiversity hot spots with high levels of endemism in deep-sea hydrothermal vents, cold seeps, and freshwater sulfide springs. The diversity of H2S-rich environments and their inhabitants provides ideal systems for comparative studies of the effects of a clear-cut source of selection across vast geographic and phylogenetic scales, ultimately informing our understanding of how environmental stressors affect ecological and evolutionary processes.

Comparative transcriptome analysis of Rimicaris sp. reveals novel molecular features associated with survival in deep-sea hydrothermal vent

“…In the category of ‘cellular component’, the upregulated subcategory of ‘extracellular region’ was significantly enriched (Fig. 4A), within this subcategory were the DGEs of chitin binding peritrophin, cuticular protein, obstructor B, gastrolith protein, and laminin (Table 3), which are involved in the synthesis of calcified cuticular structures in invertebrates that may act as barriers to prevent the entry of H 2 S into the body 9, 18 .

Figure 3Volcano plot displaying differential expressed genes (DEGs) between GR and mGR samples. The red and green dots represent upregulated and downregulated DEGs, respectively, in the GR samples; the blue dots represent non-DEGs.

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Complexities of gene expression patterns in natural populations of an extremophile fish (Poecilia mexicana, Poeciliidae)

“…). So, even though H 2 S‐rich and cave environments are often assumed to exert strong selection (Niemiller & Soares, ; Tobler et al., ), and H 2 S has specific and well‐documented biochemical and physiological effects (Olson, ), the consequences of exposure to these environments are not systemic and uniform but specific to particular organs. In the nonsulphidic cave for example, the majority of differentially expressed genes occurred in the liver (Figure ), and the enrichment in Reactome pathways differed among organs (especially gills vs. liver and brain; Fig.…”

“…). In both sulphidic habitats, differentially expressed genes were mostly concentrated in the gills (Figure ), which are directly exposed to environmental H 2 S (Tobler et al., ). Furthermore, genes associated with H 2 S detoxification and the metabolic processing of sulphur were primarily differentially expressed in the gills but not the brain or the liver.…”

“…(iii) Some sources of selection may elicit more predictable evolutionary responses than others. At least in the organs investigated here, the presence of H 2 S—unlike the absence of light—has clear‐cut molecular targets ( e.g ., cytochrome c oxidase in the respiratory chain and haemoglobin) that affect specific physiological functions (e.g., energy metabolism, oxygen transport and oxidative stress; Li et al., ; Olson, ; Tobler et al., ). H 2 S's direct interaction with specific proteins could constrain the diversity of adaptive solutions that mitigate the toxic effects, ultimately leading to more predictable outcomes in gene expression variation in replicated populations.…”

“…Indeed, previous studies have found that sulphide spring populations exhibit positive selection on and differential expression of genes associated with highly conserved pathways involved in H 2 S toxicity and detoxification (Kelley et al., ; Pfenninger et al., , ). Furthermore, the notion that H 2 S elicits more predictable organismal responses is supported by the level of shared responses between populations being disproportionally high in the gills, which are directly exposed to environmental H 2 S (Tobler et al., ). Physiochemical stressors with clear molecular targets eliciting predictable patterns of genetic evolution have also been documented in other organisms, such as killifish adapted to anthropogenic pollutants (Reid et al., ), insects adapted to secondary plant metabolites (Dobler, Dalla, Wagschal, & Agrawal, ) and poison frogs adapted to their own skin toxins (Tarvin, Santos, O'Connell, Zakon, & Cannatella, ).…”