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  1. Atmospheric carbon dioxide and oxygen concentrations are partially linked via the geological cycle of organic carbon (Fig. 1A-C; e.g., CO2 + H2O ↔ CH2O + O2). The history of these two biologically active components, controls on their concentrations, and implications for the complexity of the biosphere and habitability of Earth have been hotly debated, but generally considered independently. Ribulose bisphosphate carboxylase/oxygenase, RuBisCo, is the enzyme responsible for all oxygenic photosynthesis, carbon fixation, and is the gatekeeper of energy flow to the animal kingdom. Since RuBisCo also fixes O2 as part of photorespiration, O2 and CO2 compete for the active site of RuBisCo. Episodes of enhanced organic carbon burial contributed to removing carbon and releasing oxygen to the environment, particularly after the advent of land biota, so dramatically increased the O2/CO2 ratio (Fig. 1B). This increase in O2/CO2 should have influenced the efficiency of RuBisCo, shifting the balance towards the energy-sapping photorespiration and limiting the carbon fixation ability of plants and algae, thereby reducing new productivity and the energy cascade to the higher trophic levels within the ecosystem. However, the complexity of the modern ecosystem has emerged and thrived amidst this backdrop of increasing O2/CO2 throughout the Phanerozoic, which raises key research questions regarding evolution and habitability. To what extent can the biosphere adapt to variations caused by geological cycles? Are there Gaia-like feedbacks between life and their physical environment that assist in maintaining Earth’s habitability? Does the biosphere itself limit the range of environmental possibilities? Here we link the history of Phanerozoic O2 and CO2 concentrations and draw together the evolution of marine algal primary producers and the diversity history of marine animals to explore feedbacks between life and the environment. We emphasise that spatially resolved coupled redox and fossil evidence may be key to understanding feedbacks between the biosphere and the geosphere, as well as the drivers and limits on habitability. 
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    Free, publicly-accessible full text available March 14, 2025
  2. Two of the traits most often observed to correlate with extinction risk in marine animals are geographical range and body size. However, the relative effects of these two traits on extinction risk have not been investigated systematically for either background times or during mass extinctions. To close this knowledge gap, we measure and compare extinction selectivity of geographical range and body size of genera within five classes of benthic marine animals across the Phanerozoic using capture–mark–recapture models. During background intervals, narrow geographical range is strongly associated with greater extinction probability, whereas smaller body size is more weakly associated with greater extinction probability. During mass extinctions, the association between geographical range and extinction probability is reduced in every class and fully eliminated in some, whereas the association between body size and extinction probability varies in strength and direction across classes. While geographical range is universally the stronger predictor of survival during background intervals, variation among classes during mass extinction suggests a fundamental shift in extinction processes during these global catastrophes.

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    Free, publicly-accessible full text available September 1, 2024
  3. Abstract A central question in the study of mass extinction is whether these events simply intensify background extinction processes and patterns versus change the driving mechanisms and associated patterns of selectivity. Over the past two decades, aided by the development of new fossil occurrence databases, selectivity patterns associated with mass extinction have become increasingly well quantified and their differences from background patterns established. In general, differences in geographic range matter less during mass extinction than during background intervals, while differences in respiratory and circulatory anatomy that may correlate with tolerance to rapid change in oxygen availability, temperature, and pH show greater evidence of selectivity during mass extinction. The recent expansion of physiological experiments on living representatives of diverse clades and the development of simple, quantitative theories linking temperature and oxygen availability to the extent of viable habitat in the oceans have enabled the use of Earth system models to link geochemical proxy constraints on environmental change with quantitative predictions of the amount and biogeography of habitat loss. Early indications are that the interaction between physiological traits and environmental change can explain substantial proportions of observed extinction selectivity for at least some mass extinction events. A remaining challenge is quantifying the effects of primary extinction resulting from the limits of physiological tolerance versus secondary extinction resulting from the loss of taxa on which a given species depended ecologically. The calibration of physiology-based models to past extinction events will enhance their value in prediction and mitigation efforts related to the current biodiversity crisis. 
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  4. Rising temperatures are associated with reduced body size in many marine species, but the biological cause and generality of the phenomenon is debated. We derive a predictive model for body size responses to temperature and oxygen (O 2 ) changes based on thermal and geometric constraints on organismal O 2 supply and demand across the size spectrum. The model reproduces three key aspects of the observed patterns of intergenerational size reductions measured in laboratory warming experiments of diverse aquatic ectotherms (i.e., the “temperature-size rule” [TSR]). First, the interspecific mean and variability of the TSR is predicted from species’ temperature sensitivities of hypoxia tolerance, whose nonlinearity with temperature also explains the second TSR pattern—its amplification as temperatures rise. Third, as body size increases across the tree of life, the impact of growth on O 2 demand declines while its benefit to O 2 supply rises, decreasing the size dependence of hypoxia tolerance and requiring larger animals to contract by a larger fraction to compensate for a thermally driven rise in metabolism. Together our results support O 2 limitation as the mechanism underlying the TSR, and they provide a physiological basis for projecting ectotherm body size responses to climate change from microbes to macrofauna. For small species unable to rapidly migrate or evolve greater hypoxia tolerance, ocean warming and O 2 loss in this century are projected to induce >20% reductions in body mass. Size reductions at higher trophic levels could be even stronger and more variable, compounding the direct impact of human harvesting on size-structured ocean food webs. 
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  5. Oxygen levels in the atmosphere and ocean have changed dramatically over Earth history, with major impacts on marine life. Because the early part of Earth’s history lacked both atmospheric oxygen and animals, a persistent co-evolutionary narrative has developed linking oxygen change with changes in animal diversity. Although it was long believed that oxygen rose to essentially modern levels around the Cambrian period, a more muted increase is now believed likely. Thus, if oxygen increase facilitated the Cambrian explosion, it did so by crossing critical ecological thresholds at low O2. Atmospheric oxygen likely remained at low or moderate levels through the early Paleozoic era, and this likely contributed to high metazoan extinction rates until oxygen finally rose to modern levels in the later Paleozoic. After this point, ocean deoxygenation (and marine mass extinctions) is increasingly linked to large igneous province eruptions—massive volcanic carbon inputs to the Earth system that caused global warming, ocean acidification, and oxygen loss. Although the timescales of these ancient events limit their utility as exact analogs for modern anthropogenic global change, the clear message from the geologic record is that large and rapid CO2 injections into the Earth system consistently cause the same deadly trio of stressors that are observed today. The next frontier in understanding the impact of oxygen changes (or, more broadly, temperature-dependent hypoxia) in deep time requires approaches from ecophysiology that will help conservation biologists better calibrate the response of the biosphere at large taxonomic, spatial, and temporal scales. 
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  6. Abstract

    Larger body size has long been assumed to correlate with greater risk of extinction, helping to shape body-size distributions across the tree of life, but a lack of comprehensive size data for fossil taxa has left this hypothesis untested for most higher taxa across the vast majority of evolutionary time. Here we assess the relationship between body size and extinction using a data set comprising the body sizes, stratigraphic ranges, and occurrence patterns of 9408 genera of fossil marine animals spanning eight Linnaean classes across the past 485 Myr. We find that preferential extinction of smaller-bodied genera within classes is substantially more common than expected due to chance and that there is little evidence for preferential extinction of larger-bodied genera. Using a capture–mark–recapture analysis, we find that this size bias of extinction persists even after accounting for a pervasive bias against the sampling of smaller-bodied genera within classes. The size bias in extinction also persists after including geographic range as an additional predictor of extinction, indicating that correlation between body size and geographic range does not provide a simple explanation for the association between size and extinction. Regardless of the underlying causes, the preferential extinction of smaller-bodied genera across many higher taxa and most of geologic time indicates that the selective loss of large-bodied animals is the exception, rather than the rule, in the evolution of marine animals.

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  7. Abstract The taxonomic and ecologic composition of Earth's biota has shifted dramatically through geologic time, with some clades going extinct while others diversified. Here, we derive a metric that quantifies the change in biotic composition due to extinction or origination and show that it equals the product of extinction/origination magnitude and selectivity (variation in magnitude among groups). We also define metrics that describe the extent to which a recovery (1) reinforced or reversed the effects of extinction on biotic composition and (2) changed composition in ways uncorrelated with the extinction. To demonstrate the approach, we analyzed an updated compilation of stratigraphic ranges of marine animal genera. We show that mass extinctions were not more selective than background intervals at the phylum level; rather, they tended to drive greater taxonomic change due to their higher magnitudes. Mass extinctions did not represent a separate class of events with respect to either strength of selectivity or effect. Similar observations apply to origination during recoveries from mass extinctions, and on average, extinction and origination were similarly selective and drove similar amounts of biotic change. Elevated origination during recoveries drove bursts of compositional change that varied considerably in effect. In some cases, origination partially reversed the effects of extinction, returning the biota toward the pre-extinction composition; in others, it reinforced the effects of the extinction, magnifying biotic change. Recoveries were as important as extinction events in shaping the marine biota, and their selectivity deserves systematic study alongside that of extinction. 
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  8. Ecological differentiation is correlated with taxonomic diversity in many clades, and ecological divergence is often assumed to be a cause and/or consequence of high speciation rate. However, an analysis of 30,074 genera of living marine animals and 19,992 genera of fossil marine animals indicates that greater ecological differentiation in the modern oceans is actually associated with lower rates of origination over evolutionary time. Ecologically differentiated clades became taxonomically diverse over time because they were better buffered against extinction, particularly during mass extinctions, which primarily affected genus-rich, ecologically homogeneous clades. The relationship between ecological differentiation and taxonomic richness was weak early in the evolution of animals but has strengthened over geological time as successive extinction events reshaped the marine fauna.

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