The evolution of endothermy is explained by thyroid hormone-mediated responses to cold in early vertebrates

Abstract

The evolution of endothermy is one of the most intriguing and consistently debated topics in vertebrate biology, but the proximate mechanisms that mediated its evolution are unknown. Here, we suggest that the function of thyroid hormone in regulating physiological processes in response to cold is key to understanding the evolution of endothermy. We argue that the capacity of early chordates to produce thyroid hormone internally was the first step in this evolutionary process. Selection could then act on the capacity of thyroid hormone to regulate metabolism, muscle force production and cardiac performance to maintain their function against the negative thermodynamic effects of decreasing temperature. Thyroid-mediated cold acclimation would have been the principal selective advantage. The actions of thyroid hormone during cold acclimation in zebrafish are very similar to its role during endothermic thermogenesis. The thyroid-mediated increases in metabolism and locomotor performance in ectotherms eventually resulted in sufficient heat production to affect body temperature. From this point onwards, increased body temperature per se could be of selective advantage and reinforce thyroid-induced increases in physiological rates. Selection for increased body temperature would promote those mechanisms that maximise heat production, such as increased Na + /K + -ATPase activity, futile cycling by SERCA, and mitochondrial uncoupling, all of which are regulated by thyroid hormone. The specific end point of this broader evolutionary process would be endothermic thermoregulation. However, considering the evolution of endothermy in isolation is misleading because the selective advantages that drove the evolutionary process were independent from endothermy. In other words, without the selective advantages of thyroid-mediated cold acclimation in fish, there would be no endotherms. KEY WORDS: Thermoregulation, Locomotion, Metabolism, Heat production, Aerobic capacity IntroductionThe advantages that have led to the evolution of an endothermic physiology are still under debate. A widely accepted model is that directional selection for incremental increases in aerobic capacity and sustained activity led to the evolution of endothermy (the 'aerobic capacity' model) (Bennett and Ruben, 1979;Nespolo et al., 2011). The greater scope for physical activity means that endotherms tire less quickly and are therefore better able to forage, escape predators and migrate (Clarke and Pörtner, 2010). Increased physical activity requires a greater capacity for energy (ATP) production, and oxidative metabolic capacities of endotherms are consequently an order of magnitude greater than those of ectotherms COMMENTARY School of Biological Sciences A08, University of Sydney, NSW 2006, Australia.*Author for correspondence (frank.seebacher@sydney.edu.au) (Bennett and Ruben, 1979). In contrast, the 'parental care' model suggests that increased non-shivering thermogenesis permitted parents to control incubation temperatures and thereby provided the...

Energy Homeostasis in Monotremes

“…The contribution of the monotremes to our understanding of the evolution of endothermy is discussed later in this review, but whatever the selective process, the acquisition of endothermy appears to be closely linked to thyroid hormones (Little and Seebacher, 2014). The elevated metabolism associated with endothermy in mammals is produced by leaky cell membranes, and thyroid hormones play a key role in regulating metabolic rate by increasing leakiness and thus increasing cellular ATP turnover (Hulbert, 2000).…”

Hormones and the Evolution of Complex Traits: Insights from Artificial Selection on Behavior

“…In particular, the evolution of mammalian (and avian) endothermy has long been of interest in comparative, ecological, and evolutionary physiology (Garland and Carter 1994), but so far has escaped much scrutiny from evolutionary endocrinologists (Alberts and Pickler 2012;Little and Seebacher 2014). Kemp (2006) views the origin of mammalian endothermy as a paradigm for the evolution of complex traits.…”

Discovery of latitudinal gradient of triidothyronine concentrations in ectotherms as revealed from a cyprinid fish, the common roach Rutilus rutilus

“…Although most ectotherms do not display adaptive thermogenesis, they do acclimate cellular metabolism to compensate for environmental temperature variation (Guderley, 2004;Seebacher, 2009). Since THs are involved in adaptive metabolic responses to thermal changes by regulation of mitochondrial biogenesis (Weitzel et al, 2003;Seebacher, 2009;Little and Seebacher, 2014), significantly increased serum T 3 concentrations in the common roach in northern localities are most likely to be adaptive for the colder environment. Thyroid hormones were found to regulate thermal acclimation in ectotherms as shown in a recent experiment with zebrafish (Little et al, 2013).…”

“…We suggest that the greater increase in serum T 3 concentrations along a southenorth axis in ectotherms could be explained by intensification of cellular metabolism for adaptation to cold environments under an almost complete lack of mechanisms of thermogenesis. Thyroid-mediated cold acclimation in early vertebrates is considered as prevenient step prior to the origin of endothermy (Little and Seebacher, 2014).…”

“…Thyroid hormones are involved in stimulation of Na þ /K þ -ATPase activity in fish (Madsen and Korsgaard, 1989), a component of the cold acclimation response (Schwarzbaum et al, 1992). Recent experiments with cold water acclimated zebrafish Danio rerio (Hamilton 1822) showed THs to maintain high levels of locomotor performance, muscle function, metabolic capacity, and heart rate in response to cold (Little et al, 2013;Little and Seebacher, 2014). In fact, THs regulate cold acclimation in ectotherms using the same pathways as during thermogenesis in endotherms exposed to cold (Little and Seebacher, 2014).…”