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Convergent evolution of conserved repeated adaptation to extreme environments

Ryan Greenway, Nick Barts, Chathurika Henpita, Anthony P. Brown, Lenin Arias Rodriguez, Carlos M. Rodríguez Peña, Sabine Arndt, Gigi Y. Lau, Michael P. Murphy, Lei Wu, Dingbo Lin, Jennifer H. Shaw, Joanna L. Kelley, Michael Tobler

https://www.biorxiv.org/content/10.1101/2020.02.24.959916v1

Article now published in Proceedings of the National Academy of Sciences at http://dx.doi.org/10.1073/pnas.2004223117

Multiple lineages of poecilid fish have colonized one of Earth’s most extreme environments – hydrogen sulphide (H2S) springs. How, you ask? Greenway et al. reveal that convergent mitochondrial adaptations conferred H2S tolerance to each lineage.

Selected by Giulia Rossi

Background

For decades, biologists have been captivated by organisms living in Earth’s most inhospitable environments. These organisms, known as extremophiles, provide valuable clues about the adaptations that facilitate survival at the edges of existence. For example, the evolution of antifreeze glycoproteins has allowed notothenioid fishes to persist in Antarctica’s frigid waters (Chen et al., 1997), whereas specialized hairs that reflect near-infrared light – wavelengths at which the sun is hottest – have allowed Saharan ants to tolerate scorching desert temperatures (Shi et al., 2015). While the study of extremophilic organisms has revealed many remarkable adaptations, it is unclear whether the repeated colonization of an extreme environment would be facilitated by the same evolutionary innovation each time. In other words, if we replayed the “tape of life” over and over, would we always get the same evolutionary outcome?

The invasion of sulphidic aquatic environments by several independent lineages of live-bearing fishes (Poeciliidae) provides an excellent opportunity to examine this question. Hydrogen sulphide (H2S) is an extreme environmental stressor because it impairs mitochondrial respiration and the aerobic production of ATP (Cooper and Brown 2008; Cochrane et al., 2019). Nevertheless, multiple poecilid lineages have colonized H2S-rich springs, and independently evolved H2S tolerance. Greenway et al. used three population pairs of Poecilia mexicana from adjacent sulphidic and non-sulphidic habitats to examine whether convergent modifications to mitochondrial enzymes – cytochrome c oxidase (COX; the primary toxicity target) and sulphide: quinone oxidoreductase (SQR; a major detoxification enzyme) – have allowed fish to persist in these extreme aquatic environments.

 Key Findings

Greenway et al. hypothesized that if COX resistance to H2S was the primary mechanism of H2S tolerance, then H2S exposure would not impair COX function in fish from sulphidic springs. Interestingly, exposure to H2S did not alter COX activity in fish from two of the three sulphidic populations, indicating that H2S resistance may contribute to tolerance in some P. mexicanapopulations, but not others. Not surprisingly, exposure to H2S inhibited COX activity in all three non-sulphidic populations.

The authors also investigated whether fish from sulphidic springs had a greater capacity for H2S detoxification. In the face of H2S exposure, all three sulphidic populations exhibited higher SQR activity than their non-sulphidic counterparts, indicating that H2S detoxification by the mitochondria likely contributes to H2S tolerance. The authors corroborated this finding by exposing fish to elevated H2S, and then measuring H2S in the mitochondria of various organs (e.g., liver). Lower H2S concentrations were measured in the mitochondria of fish from sulphidic populations, which is also suggestive of enhanced detoxification.

 Since mitochondrial adaptations likely underpin the enhanced H2S tolerance of P. mexicana from sulphide springs, Greenway et al. hypothesized that mitochondrial function in these fish should be maintained upon exposure to H2S. The authors isolated mitochondria from all six P. mexicana populations, and compared mitochondrial function (i.e., basal respiration, maximal respiration, and spare respiratory capacity). In support of their hypothesis, the mitochondria of H2S-tolerant fish continue to produce ATP in the presence of H2S, whereas the mitochondrial function in non-sulphidic populations was greatly reduced.

 Finally, Greenway et al. used 10 independent lineages of sulphide spring fishes across multiple genera of Poeciliidae to assess the expression of genes involved with H2S toxicity and detoxification. Overall, 186 genes exhibited convergent expression shifts in sulphide spring fishes, reiterating that convergent mitochondrial adaptations enabled multiple poecilid fish lineages to colonize H2S-rich environments.

What I liked most about this pre-print

 In 1929, August Krogh famously stated that “For a large number of problems there will be some animal of choice, or a few such animals, on which it can be most conveniently studied”. As a comparative physiologist, Krogh presumably intended this concept – known as Krogh’s principle – to apply to animal physiology. In their pre-print,Greenway et al. elegantly demonstrated that Krogh’s principle also has applications in evolutionary biology. The authors used an ideal biological system to ask novel questions about the evolution of traits underpinning the survival of fishes in one of Earth’s harshest environments.

I also admire how the authors used multiple approaches to verify the findings of their study. For example, SQR enzyme activities indicated that fish from sulphidic populations had a greater H2S detoxification capacity than fish from non-sulphidic populations. The authors corroborated this finding with in vivo H2S measurements, as well as gene expression data.

Questions for the Authors

  1. Would you expect similar mitochondrial adaptations in animals that occupy other H2S-rich environments (e.g., hydrothermal vents)? Alternatively, do you think different taxa are likely to use different adaptations despite the similar selection pressures imposed by elevated H2S?

 

  1. Unlike H2S, many environmental stressors do not have specific toxicity targets. If multiple P. mexicana lineages had colonized thermally extreme environments, would you expect the same adaptation(s) conferring thermal tolerance to have evolved independently across the lineages?

 

  1. Behavioural adaptations, such as aquatic surface respiration, can play an important role in allowing P. mexicana to persist in sulphidic environments (Plath et al., 2007). If some P. mexicana populations rely more heavily on behaviour than others, do you think it would relax the pressure to evolve physiological tolerance?

Additional References

 Chen, L., Devries, A.L., Cheng, C.-H.C. (1997) Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. P. Natl. Acad. Sci. USA. 94, 3811-3816.

Cochrane, P.V., Rossi, G.S., Tunnah, L., Jonz, M.G., Wight, P.A. (2019) Hydrogen sulphide toxicity and the importance of amphibious behaviour in a mangrove fish inhabiting sulphide-rich habitats. J. Comp. Physiol. B. 189, 223-235.

Cooper, C.E., Brown, G.C. (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J. Bioenerg. Biomembr. 40, 533-539.

Plath, M., Tobler, M., Riesch, R., Garcia de Leon, F.J., Giere, O., Schlupp, I. (2007) Survival in an extreme habitat: the role of behaviour and energy limitation. Naturwissenschaften. 94, 991-996.

Shi, N.N., Tsai, C.-C., Camino, F., Bernard, G.D., Yu, N., Wehner, R. (2015) Keeping cool: Enhanced optical reflection and radiative heat dissipation in Saharan silver ants. Science. 349, 298-301.

 

Posted on: 26th March 2020

doi: https://doi.org/10.1242/prelights.17913

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  • 1 comment

    3 months

    Ryan Greenway and Nick Barts

    Answers from the Authors

    1. Given the biochemical and physiological constraints that H2S places on mitochondrial and organismal function, it is tempting to predict that most organisms inhabiting H2S-rich environments would adapt in similar ways. Evidence suggests that this may sometimes be true. For example, at least three evolutionarily independent lineages of deep-sea decapod crustaceans (including crabs, squat lobsters, and shrimps) all exhibit evidence for positive selection acting on mitochondrial OxPhos genes [1], just as we found across poeciliid fishes. In addition, other animals from H2S-rich habitats exhibit high detoxification activity through SQR, although the evolutionary context of these patterns often remain elusive because comparisons to susceptible organisms either are missing or involve distantly related species with vast differences in genomic architectures and body plans [2,3]. It is important to note, however, that organisms have evolved a suite of additional solutions to cope with chronic sulfide-induced stress. There are four primary mechanisms that may facilitate survival in sulfidic environments, including behavioral avoidance, mitigation of negative effects imposed on toxicity targets, regulation of internal sulfide concentrations, and symbioses with chemosynthetic bacteria, which are outlined in more detail in Tobler et al. 2016 [4].

    2. Toxicants – both naturally occurring and anthropogenic – are great for studying evolutionary responses precisely because they have clear, specific targets, and we often have a good understanding of the physiological and biochemical pathways affected by these substances. This knowledge has provided great opportunities to investigate adaptations across levels of biological organization and among divergent lineages. Aside from our preprint on poeciliids adapting to H2S, similar approaches have been used to study how Fundulus killifishes have repeatedly evolved tolerance to hydrocarbon pollutants [5] and how divergent lineages of snakes can tolerate tetrodotoxin that naturally occurs in their amphibian prey [6]. One big take-away from these studies is that the high specificity of toxicants often means there are fewer ways organisms can adapt, constraining evolutionary solutions and enabling us to make predictions about the molecular bases of adaptation in these systems. The more specific the targets, the more likely it is that evolution repeats itself. Other abiotic stressors, like temperature, affect a broader set of processes and pathways simultaneously, likely resulting in lower repeatability of adaptation across increasingly divergent lineages.

    3.This is an excellent question! Understanding the role of behavior and physiology in adaptation is of interest to many biologists, as they may act independently or interact to facilitate survival under novel conditions. One hypothesis is that organisms may need to rely only on either physiology or behavior to survive, and under this scenario we would predict that a population of P. mexicana that relies more heavily on aquatic surface respiration may experience relaxed selection on physiological mechanisms of tolerance. Alternatively, behavior and physiology may have additive effects on organisms, such that physiology and behavior are both necessary to survive under hostile conditions. This is currently a question we are tackling in the lab. Sulfidic populations of P. mexicana are an ideal system to study this question due to differences in their ability to maintain function of OxPhos under sulfide exposure in the laboratory. We predict that this species relies on both physiology and behavior to survive in sulfidic environments, and we hope to identify differences in survivability and gene expression under hypoxic and sulfidic conditions to elucidate what role each of these strategies play.

    [1] Sun S, Sha Z, and Wang Y. “Divergence history and hydrothermal vent adaptation of decapod crustaceans: A mitogenomic perspective.” PLOS ONE 14 (2019): e0224373.

    [2] Hildebrandt TM and Grieshaber M. “Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria.” FEBS J. 275 (2008): 3352–61.

    [3] Ma YB, Zhang ZF, Shao MY, Kang KH, Shi XL, Dong YP, and Li JJ. “Response of sulfide-quinone oxidoreductase to sulfide exposure in the echiuran worm Urechis unicinctus.” Marine Biotechnology 14 (2012): 245–51.

    [4] Tobler M, Passow CN, Greenway R, Kelley JL, and Shaw JH. “The evolutionary ecology of animals inhabiting hydrogen sulfide–rich environments.” Annual Review of Ecology, Evolution, and Systematics 47 (2016): 239-262.

    [5] Reid NM, Proestou DA, Clark BW, Warren WC, Colbourne JK, Shaw JR, Karchner SI, Hahn ME, Nacci D, Oleksiak MF, and Crawford DL. “The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish.” Science 354.6317 (2016): 1305-1308.

    [6] Feldman CR, Brodie ED, and Pfrender ME. “Constraint shapes convergence in tetrodotoxin-resistant sodium channels of snakes.” Proceedings of the National Academy of Sciences 109.12 (2012): 4556-4561.

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