Convergent evolution of conserved repeated adaptation to extreme environments
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.Giulia Rossi
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.
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
- 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?
- 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?
- 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?
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: 26 March 2020Read preprint