Harnessing hypoxia as an evolutionary driver of complex multicellularity

Abstract

Animal tissue requires low-oxygen conditions for its maintenance. The need for low-oxygen conditions contrasts with the idea of an evolutionary leap in animal diversity as a result of expanding oxic conditions. To accommodate tissue renewal at oxic conditions, however, vertebrate animals and vascular plants demonstrate abilities to access hypoxia. Here, I argue that multicellular organisms sustain oxic conditions first after internalizing hypoxic conditions. The ‘harnessing’ of hypoxia has allowed multicellular evolution to leave niches that were stable in terms of oxygen concentrations for those where oxygen fluctuates. Since oxygen fluctuates in most settings on Earth's surface, the ancestral niche would have been a deep marine setting. The hypothesis that ‘large life’ depends on harnessing hypoxia is illustrated in the context of conditions that promote the immature cell phenotype (stemness) in animal physiology and tumour biology and offers one explanation for the general rarity of diverse multicellularity over most of Earth's history.

Evolution of a key enzyme of aerobic metabolism reveals Proterozoic functional subunit duplication events and an ancient origin of animals

“…Dates of emergence of animal-specific NAD-IDH subunit β (~ 1249 Ma) and NAD-IDH subunit γ (~ 1532 Ma) provide support for an earlier emergence of metazoans compared to previous estimates that date their origin to ~ 800 Ma 71 , 72 . If animal divergence began in the Mesoproterozoic or even later in the Neoproterozoic, as suggested by recent molecular estimates 26 , 35 , 73 , hypoxic conditions should have prevailed in most environmental settings for more than half of animal evolutionary history 74 . An alternative scenario could be the existence of oxygenic niches present at the microscale since the rise of oxidative photosynthesis about 3.0 Ga 74 , 75 .…”

“…If animal divergence began in the Mesoproterozoic or even later in the Neoproterozoic, as suggested by recent molecular estimates 26 , 35 , 73 , hypoxic conditions should have prevailed in most environmental settings for more than half of animal evolutionary history 74 . An alternative scenario could be the existence of oxygenic niches present at the microscale since the rise of oxidative photosynthesis about 3.0 Ga 74 , 75 . In spite of the strong debate surrounding those conditions 76 – 79 , the fact is that hypoxic niches may have prevailed for most of Earth’s history.…”

The origin and rise of complex life: progress requires interdisciplinary integration and hypothesis testing

“…Hammarlund [64] presents a new take on the role of oxygen in early animal evolution. Rather than viewing increased oxicity of Neoproterozoic environments as having released a constraint on size and complexity in animal evolution, she presents this same biogeochemical transition as a hurdle that early animals and their forebears had to overcome.…”

The issues with tissues: the wide range of cell fate separation enables the evolution of multicellularity and cancer

“…Both the initial hyperspeciation of animals and plants and hyperspeciation events after numerous mass extinctions can be argued to associate with circumstances where either environmental or biological conditions are in flux, i.e. varying ocean chemistry [75] or predation pressure [76]. The recovery after mass extinction may resemble a relapse in cancer rather than a revolutionary organismal event, and both may demonstrate how populations with traits of phenotypic toggling and evolvability hold the evolutionary advantage under dynamic settings.…”