Convergent evolution of conserved mitochondrial pathways underlies repeated adaptation to extreme environments

Abstract

Extreme environments test the limits of life; yet, some organisms thrive in harsh conditions. Extremophile lineages inspire questions about how organisms can tolerate physiochemical stressors and whether the repeated colonization of extreme environments is facilitated by predictable and repeatable evolutionary innovations. We identified the mechanistic basis underlying convergent evolution of tolerance to hydrogen sulfide (H2S)—a toxicant that impairs mitochondrial function—across evolutionarily independent lineages of a fish (Poecilia mexicana, Poeciliidae) from H2S-rich springs. Using comparative biochemical and physiological analyses, we found that mitochondrial function is maintained in the presence of H2S in sulfide spring P. mexicana but not ancestral lineages from nonsulfidic habitats due to convergent adaptations in the primary toxicity target and a major detoxification enzyme. Genome-wide local ancestry analyses indicated that convergent evolution of increased H2S tolerance in different populations is likely caused by a combination of selection on standing genetic variation and de novo mutations. On a macroevolutionary scale, H2S tolerance in 10 independent lineages of sulfide spring fishes across multiple genera of Poeciliidae is correlated with the convergent modification and expression changes in genes associated with H2S toxicity and detoxification. Our results demonstrate that the modification of highly conserved physiological pathways associated with essential mitochondrial processes mediates tolerance to physiochemical stress. In addition, the same pathways, genes, and—in some instances—codons are implicated in H2S adaptation in lineages that span 40 million years of evolution.

Sequencing platform shifts provide opportunities but pose challenges for combining genomic data sets

“…However, for molecular ecologists working on nonmodel species, budgets still limit the amount of sequence data that can be produced. As a result, exhaustive experimental designs, which include the sampling of many individuals from many different populations, are rare (but are emerging; (Feulner et al, 2015; Greenway et al, 2020; Martin et al, 2016; Soria‐Carrasco et al, 2014; Stankowski et al, 2019; Vijay et al, 2016)). The effort to publicly archive sequence data that has already contributed to publications helps to maintain the reproducibility of sequencing studies, whilst prolonging the value of such sequence data in perpetuity.…”

“…For example, Zhang et al (2020) compiled a comprehensive data set of 365 species of asterids representing all 17 orders containing published and newly sequenced whole genomes and transcriptomes to resolve the deep asterid phylogeny. In another example, Greenway et al (2020) focus on the Poeciliidae family of fish, to demonstrate that adaptation to extreme, here sulphide‐rich, environments has evolved convergently in ten independent lineages, by combining already published and newly sequenced transcriptome sequences. Microevolutionary studies investigating spatial variation across populations or closely related taxa. Such studies typically focus on one study system but rely on a larger sampling to reflect the variation within species or populations.…”

Diurnal Changes in Hypoxia Shape Predator-Prey Interaction in a Bird-Fish System

“…If temperature conditions were as high as in the present study, due to an increase in oxygen demand we would expect this species to rely on ASR at even higher DO concentrations. Hence, it is intriguing that, despite warm water temperatures, sulphur mollies do not seem to rely much on ASR at values above 2 mg/L and may in fact convey that many adaptations to tolerate hydrogen sulfide also improve hypoxic tolerance [especially morphological adaptations facilitating oxygen acquisition (Tobler and Hastings, 2011;, upregulation of oxygen transport genes (Barts et al, 2018), shifts toward anaerobic metabolism (Kelley et al, 2016) and reduced energy demand (Passow et al, 2017;Camarillo et al, 2020) as well as modulations of pathways maintaining mitochondrial function and aerobic ATP production (Pfenninger et al, 2014;Tobler et al, 2018;Greenway et al, 2020)].…”

“…The Baños del Azufre spring complex is inhabited by the endemic sulphur molly (P. sulphuraria) that shows distinct adaptations to these severe hypoxic and sulfidic conditions (for details see Plath et al, 2007;Riesch et al, 2010b;Tobler and Hastings, 2011;Tobler et al, , 2018Pfenninger et al, 2014;Kelley et al, 2016;Brown et al, 2017;Barts et al, 2018;Camarillo et al, 2020;Greenway et al, 2020). Most notably, fish spend a majority of their time performing aquatic surface respiration (ASR), but frequently dive to engage in benthic foraging as well as aggressive or reproductive activities under water (Tobler et al, 2009).…”

“…In the case of our study species, the sulphur molly Poecilia sulphuraria, sulfidic and non-sulfidic lineages genetically diverged between 15 and 30 ky ago (Greenway, 2019). While several morphological and physiological adaptations allow this species to persist in these conditions (e.g., mouth and gill area enlargement for enhanced oxygen uptake, modified toxicity targets and detoxification pathways; Tobler and Hastings, 2011;Greenway et al, 2020), they are still dependent on aquatic surface respiration (ASR) for survival. A previous study estimated that sulphur mollies spend up to 84% of their time performing ASR (Tobler et al, 2009), which was three times higher than a closely related species (Poecilia mexicana) from a nearby (slightly less) sulfidic spring system.…”