doi: 10.1016/j.xinn.2024.100618. eCollection 2024 May 6.
Respiratory protein-driven selectivity during the Permian-Triassic mass extinction
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- PMID:38638583
- PMCID: PMC11025005
- DOI: 10.1016/j.xinn.2024.100618
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Respiratory protein-driven selectivity during the Permian-Triassic mass extinction
Haijun Song et al. Innovation (Camb)..
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Abstract
Extinction selectivity determines the direction of macroevolution, especially during mass extinction; however, its driving mechanisms remain poorly understood. By investigating the physiological selectivity of marine animals during the Permian-Triassic mass extinction, we found that marine clades with lower O2-carrying capacity hemerythrin proteins and those relying on O2 diffusion experienced significantly greater extinction intensity and body-size reduction than those with higher O2-carrying capacity hemoglobin or hemocyanin proteins. Our findings suggest that animals with high O2-carrying capacity obtained the necessary O2 even under hypoxia and compensated for the increased energy requirements caused by ocean acidification, which enabled their survival during the Permian-Triassic mass extinction. Thus, high O2-carrying capacity may have been crucial for the transition from the Paleozoic to the Modern Evolutionary Fauna.
© 2024 The Author(s).
Conflict of interest statement
The authors declare no competing interests.
Figures
Extinction and body-size reduction of marine animals at the genus level during the Permian-Triassic mass extinction (A) Extinction magnitudes of major marine clades. (B) Correlation between the proportion of extinction and O2 capacity for marine clades. (C) Correlation between the proportion of extinction and O2 capacity for animals with carbonate shells. (D) Size reduction of major marine clades. (E) Correlation between size reduction and O2 capacity for marine clades. (F) Correlation between size reduction and O2 capacity for animals with carbonate shells. Vertical bars represent binomial 95% confidence intervals for (A)–(C). Vertical bars in (D)–(F) represent the standard deviation, which was calculated from 1,000 bootstrap replicates of median size reduction. Diff (orange color), Hr (purple color), Hc (blue color), and Hb (magenta color) represent different types of animals that use diffusion, hemerythrin, hemocyanin, and hemoglobin, respectively, to transport O2 from the surroundings to their bodies. Bivalve-p and bivalve-non p represent protobranchia bivalve and hemoglobin non-protobranchia bivalve, respectively. Dashed lines and shades represent linear regression lines and their 95% confidence intervals. For the methods used to calculate extinction and size reduction and their error bars, see the supplemental materials and methods.
Extinction and size reduction in different groups (A) Differences in extinction between animals with open and closed circulatory systems in the Hc group. The open circulatory system bin includes brachiopods, ostracods, gastropods, and non-protobranchia bivalves; the closed circulatory system bin includes cephalopods. (B) Differences in extinction between animals with three O2-carrying proteins in the open circulatory system group. The Hr bin includes brachiopods; the Hc bin includes ostracods, gastropods, and protobranchia bivalves; and the Hb bin includes non-protobranchia bivalves. (C) Differences in size reduction between animals with open and closed circulatory systems in the Hc group. The open circulatory system bin includes ostracods and gastropods; the closed circulatory system bin includes cephalopods. (D) Differences in size reduction between animals with three O2-carrying proteins in the open circulatory system group. The Hr bin includes brachiopods; the Hc bin includes ostracods and gastropods; and the Hb bin includes non-protobranchia bivalves. Vertical bars represent the 95% confidence intervals for (A) and (B) and standard deviation for (C) and (D). Hr, Hc, and Hb represent hemoglobin, hemocyanin, and hemoglobin, respectively.
Logistic regression shows the selectivity of extinction during the Permian-Triassic crisis (A) Regression coefficients of extinction. Low O2-carrying capacity, narrow geographic range, motile, and physiologically unbuffered genera preferentially went extinct. Selectivity among genera with carbonate shells and a smaller number of occurrences was not significant. (B) Regression coefficients of extinction with O2-carrying capacity as categorical covariates. OCC, O2-carrying capacity. Vertical bars in (A) represent the standard errors of the regression coefficients. ∗∗∗p < 0.001 and ∗∗p < 0.01, NS, not significant. For the predictor variables and extinction status, see Table S3, and detailed results of logistic regression are shown in Tables S4–S5.
Ocean O2, H2S, and pH changes during the Permian-Triassic extinction using the cGENIE model and geological records (A and B) Subsurface redox conditions in the late Permian and earliest Triassic. (C) The difference in dissolved O2 (ΔO2) between the late Permian and earliest Triassic. (D and E) Subsurface hydrogen sulfide concentrations in the late Permian and earliest Triassic. (F) The difference in hydrogen sulfide (ΔH2S) between the late Permian and earliest Triassic. (G and H) Subsurface pH values in the late Permian and earliest Triassic. (I) The difference in pH values (ΔpH) between the late Permian and earliest Triassic. We also test other levels of ocean phosphate concentrations in the earliest Triassic (see Figures S5‒S7). Model results for dissolved O2, H2S, and pH are superimposed by observed proxy data (circles). The solid and hollow circles represent the occurrences of anoxia/hypoxia, euxinia, and acidification or not, respectively (see more information in Table S10).
References
- Knoll A.H., Bambach R.K., Payne J.L., et al. Paleophysiology and end-Permian mass extinction. Earth Planet Sci. Lett. 2007;256(3–4):295–313. doi: 10.1016/j.epsl.2007.02.018. - DOI
- Dal Corso J., Song H., Callegaro S., et al. Environmental crises at the Permian–Triassic mass extinction. Nat. Rev. Earth Environ. 2022;3(3):197–214. doi: 10.1038/s43017-021-00259-4. - DOI
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