Oxygen, temperature and the deep-marine stenothermal cradle of Ediacaran evolution

Abstract

Ediacaran fossils document the early evolution of complex megascopic life, contemporaneous with geochemical evidence for widespread marine anoxia. These data suggest early animals experienced frequent hypoxia. Research has thus focused on the concentration of molecular oxygen (O 2 ) required by early animals, while also considering the impacts of climate. One model, the Cold Cradle hypothesis, proposed the Ediacaran biota originated in cold, shallow-water environments owing to increased O 2 solubility. First, we demonstrate using principles of gas exchange that temperature does have a critical role in governing the bioavailability of O 2 -but in cooler water the supply of O 2 is actually lower. Second, the fossil record suggests the Ediacara biota initially occur approximately 571 Ma in deepwater facies, before appearing in shelf environments approximately 555 Ma. We propose an ecophysiological underpinning for this pattern. By combining oceanographic data with new respirometry experiments we show that in the shallow mixed layer where seasonal temperatures fluctuate widely, thermal and partial pressure (pO 2 ) effects are highly synergistic. The result is that temperature change away from species-specific optima impairs tolerance to low pO 2 . We hypothesize that deep and particularly stenothermal (narrow temperature range) environments in the Ediacaran ocean were a physiological refuge from the synergistic effects of temperature and low pO 2 .

Surfing in and on microbial mats: Oxygen-related behavior of a terminal Ediacaran bilaterian animal

“…We hypothesize that the in-and-out behavior was an evolutionary innovation driven by the dynamic redox conditions in both the water column and the microbial mat. Dynamic redox conditions were a challenge for early animals (Boag et al, 2018), but this challenge could be mitigated by mobile bilaterians with the capability to explore dynamic and localized O 2 oases, which together with the heterogenic distribution of food (Budd and Jensen, 2017), may have been a stimulus for the evolution of animal mobility. This hypothesis can be further tested through a comprehensive analysis of terminal Ediacaran trace fossils exhibiting potential signs of in-and-out behavior (Jensen et al, 2000;Jensen and Runnegar, 2005;Meyer et al, 2014) to demonstrate the global scale of this innovation.…”

On the co‐evolution of surface oxygen levels and animals

“…More likely, temperature played an important role through its effects on oxygen demand. An animal's oxygen demand increases at both higher and lower temperatures than its temperature optima due to effects on oxygen supply and ventilation costs in the cold spectrum and effects on metabolic rate in the warm spectrum (Boag, Stockey, Elder, Hull, & Sperling, ; Pörtner, ). In other words, animals die at higher temperatures not because of any direct effect of temperature, but because their metabolic rates are so high they are literally suffocating.…”

“…This also means an organism does not have a static oxygen tolerance, but its tolerance is temperature‐related through effects on both supply and demand. The synergistic effects of O 2 and temperature are only starting to be explored with respect to early animal evolution (Boag et al, ; Reinhard et al, ), and temperature estimates for the Proterozoic are scarce or unreliable. These are obvious areas for future research.…”

Harnessing hypoxia as an evolutionary driver of complex multicellularity

“…This vulnerability would make them unlikely to survive in Earth's shallow marine niches, where oxygen concentrations continuously fluctuate as a result of wind, temperature and primary production (figure 6). One geological observation of proto-animals are the Ediacaran organisms found in deep marine settings [108,110]. Their occurrence is biased by preservation, but a deep marine setting [111] would be consistent with the prediction that primitive stemness control demands an environment with stable oxygen concentrations.…”