A phenology of the evolution of endothermy in birds and mammals

Abstract

Recent palaeontological data and novel physiological hypotheses now allow a timescaled reconstruction of the evolution of endothermy in birds and mammals. A three-phase iterative model describing how endothermy evolved from Permian ectothermic ancestors is presented. In Phase One I propose that the elevation of endothermy - increased metabolism and body temperature (T ) - complemented large-body-size homeothermy during the Permian and Triassic in response to the fitness benefits of enhanced embryo development (parental care) and the activity demands of conquering dry land. I propose that Phase Two commenced in the Late Triassic and Jurassic and was marked by extreme body-size miniaturization, the evolution of enhanced body insulation (fur and feathers), increased brain size, thermoregulatory control, and increased ecomorphological diversity. I suggest that Phase Three occurred during the Cretaceous and Cenozoic and involved endothermic pulses associated with the evolution of muscle-powered flapping flight in birds, terrestrial cursoriality in mammals, and climate adaptation in response to Late Cenozoic cooling in both birds and mammals. Although the triphasic model argues for an iterative evolution of endothermy in pulses throughout the Mesozoic and Cenozoic, it is also argued that endothermy was potentially abandoned at any time that a bird or mammal did not rely upon its thermal benefits for parental care or breeding success. The abandonment would have taken the form of either hibernation or daily torpor as observed in extant endotherms. Thus torpor and hibernation are argued to be as ancient as the origins of endothermy itself, a plesiomorphic characteristic observed today in many small birds and mammals.

Modelling mammalian energetics: the heterothermy problem

“…Conversely, in colder climates where most small-bodied species rest in thermally insulated burrows, diurnal activity can reduce overall energy expenditure by lowering the need for thermogenesis during the active period [13,62]. The relative energetic costs and benefits of a nocturnal or diurnal activity pattern have so far mostly been discussed in single species studies, or in hypotheses about the evolution of endothermy [40,61,[63][64][65]. Unfortunately, nocturnal and diurnal species, as well as those that do not fit clearly in either category, are usually lumped together in meta-analyses despite facing vastly different environmental conditions.…”

“…Energy usage in relation to climate is further affected by phylogeny, activity level, microclimate selection, reproductive status, and energy availability [13,21,[37][38][39][40]. Due to fundamental differences in thermoregulation between mammals and birds, we will focus predominantly on mammals in this review (but see [32,35,41] for a discussion on birds).…”

The role of the red blood cell and platelet in the evolution of mammalian and avian endothermy

“…The evolution of endothermy in mammals and birds from their ectothermic ancestors occurred over a period of millions of years and was the culmination of a continuum of genetic modifications (Grigg, Beard, & Augee, ; Lovegrove, ; Polymeropoulos, Oelkrug, & Jastroch, ). These genetic alterations were structural changes in skeletal and soft tissue elements, such as the evolution of the four‐chambered heart, along with molecular modifications.…”

“…Endotherms are able to maintain an elevated basal metabolic rate (BMR), and elevated metabolic rates for sustained muscle activity and locomotion at all times of the day, mammals have lactate‐producing mammary tissue for parenting, provide consistent body warmth with optimal enzyme activity, have enhanced encephalization, and can move into broader ecological niches (Bennett & Ruben, ; Grigg et al, ; Isler & van Schaik, ; Lovegrove, ; Polymeropoulos et al, ; Rowe, Macrini, & Luo, ). However, it should be noted that ectotherms have several mechanisms to elevate their body temperature above ambient temperatures and many endotherms have body temperatures that fluctuate significantly during daily torpor and during periods of hibernations (Lovegrove, ). Ectotherms may modulate their body temperature by regulating heat loss/retention by increasing/decreasing blood flow through their periphery (Porter & Witmer, ).…”

Thermoregulation in free‐ranging ground woodpeckers Geocolaptes olivaceus: no evidence of torpor

“…Endothermy evolved independently in birds and mammals (Ruben 1995, Lovegrove 2016. The elevated energy demands associated with endothermic homeothermy, particularly in cold environments, have led to both classes evolving a number of behavioural and physiological mechanisms of energy conservation.…”