Improved heat tolerance in air drives the recurrent evolution of air-breathing

Abstract

The transition to air-breathing by formerly aquatic species has occurred repeatedly and independently in fish, crabs and other animal phyla, but the proximate drivers of this key innovation remain a long-standing puzzle in evolutionary biology. Most studies attribute the onset of air-breathing to the repeated occurrence of aquatic hypoxia; however, this hypothesis leaves the current geographical distribution of the 300 genera of air-breathing crabs unexplained. Here, we show that their occurrence is mainly related to high environmental temperatures in the tropics. We also demonstrate in an amphibious crab that the reduced cost of oxygen supply in air extends aerobic performance to higher temperatures and thus widens the animal's thermal niche. These findings suggest that high water temperature as a driver consistently explains the numerous times air-breathing has evolved. The data also indicate a central role for oxygen-and capacity-limited thermal tolerance not only in shaping sensitivity to current climate change but also in underpinning the climate-dependent evolution of animals, in this case the evolution of air-breathing.

Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology

“…In contrast, crustaceans still use their gills when in air and are therefore suitable models to investigate the potential benefits of air breathing for thermal tolerance. In fact, findings in amphibious crabs corroborate that oxygen supply costs are reduced in air and that this causes enhanced heat tolerance (Giomi et al, 2014). Insects may also have exploited this route; while aquatic larvae are subject to OCLTT principles (Verberk and Calosi, 2012), the tracheal oxygen supply to tissues in terrestrial adults supports elevated heat tolerance at minimised oxygen-supply costs.…”

“…2). Increasing ambient oxygen levels can lower the slope of the exponential rise in SMR and cause significantly lowered oxygen consumption rates at high temperatures -as seen in resting fish (Mark et al, 2002) or in amphibious crabs exposed to air (Giomi et al, 2014) -thereby increasing T c . Excess oxygen leads to reduced blood flow and thus lowers the cost of cardiovascular activity.…”

“…Pörtner et al, 2005;Knoll et al, 2007). It has been suggested to be an early evolutionary principle in animals that has been modified according to life stage (see Pörtner and Farrell, 2008) or climate zone (Pörtner, 2006;Beers and Sidell, 2011;Pörtner et al, 2013), or during the evolution of air breathing (Giomi et al, 2014).…”

“…The basic idea underlying the OCLTT is that once temperatures approach limiting values, constraints on the capacity of an animal to supply oxygen to tissues to meet demand cause a progressive decline in performance (e.g. Pörtner and Giomi et al, 2014), with consequences at the ecosystem level (e.g. Del Raye and Weng, 2015;Payne et al, 2016).…”

Oxygen safety margins set thermal limits in an insect model system

“…two-stage gas exchange, discussed in Klok et al, 2004), the respiratory milieu (e.g. Giomi et al, 2014;reviewed in Hsia et al, 2013) and the degree to which an animal is capable of regulating its gas exchange at rest, especially in the face of changing oxygen availability, may explain the difference between marine invertebrates that show support for OCLTT and air-breathing invertebrates that generally do not (Verberk and Bilton, 2013). For example, Verberk and Bilton (2013) showed across four insect orders that the degree of respiratory control within a particular species determined the extent of the oxygen limitation [measured as a reduction in critical thermal maximum (CT max ) with hypoxia].…”