Since the Eocene, the diversity of artiodactyls has increased while that of perissodactyls has decreased. Reasons given for this contrasting pattern are that the evolution of a ruminant digestive tract and improved locomotion in artiodactyls were adaptively advantageous in the highly seasonal post-Eocene climate. We suggest that evolution of a carotid rete, a structure highly developed in artiodactyls but absent in perissodactyls, was at least as important. The rete confers an ability to regulate brain temperature independently of body temperature. The net effect is that in hot ambient conditions artiodactyls are able to conserve energy and water, and in cold ambient conditions they are able to conserve body temperature. In perissodactyls, brain and body temperature change in parallel and thermoregulation requires abundant food and water to warm/cool the body. Consequently, perissodactyls occupy habitats of low seasonality and rich in food and water, such as tropical forests. Conversely, the increased thermoregulatory flexibility of artiodactyls has facilitated invasion of new adaptive zones ranging from the Arctic Circle to deserts and tropical savannahs.

0.8±0.1°C. There were daily variations of up to 2.3°C in carotid body temperature in individual animals. An average range of carotid blood temperature of 3.1±0.4°C over the study period was recorded for the group, which was significantly wider than the average variation in brain temperature (2.3±0.6°C). Minimum carotid temperature (36.4±0.8°C) was significantly lower than minimum brain temperature (37.7±0.5°C), but maximum brain and carotid temperatures were similar. Brain temperature was kept relatively constant by a combination of warming at low carotid temperatures and cooling at high carotid temperatures and so varied less than carotid temperature. This regulation of brain temperature may be the origin of the amplitude of the average variation in carotid temperature found, and may confer a survival advantage.

SUMMARYConservation of energy is a prerequisite thermoregulatory strategy for survival in northern hemisphere winters. We have used thermistor/data logger assemblies to measure temperatures in the brain, carotid artery, jugular vein and abdominal cavity, in pronghorn antelope to determine their winter body temperature and to investigate whether the carotid rete has a survival role. Over the study period mean black globe and air temperature were -0.5±3.2°C and -2.0±3.4°C, respectively, and mean daytime solar radiation was ~186·W·m -2 . Brain temperature (T brain , 39.3±0.3°C) was higher than carotid blood temperature (T carotid , 38.5±0.4°C), and higher than jugular temperature (T jugular , 37.9±0.7°C). Minimum T brain (38.5±0.4°C) and T carotid (37.8±0.2°C) in winter were higher than the minimum T brain (37.7±0.5°C) and T carotid (36.4±0.8°C) in summer that we have reported previously. Compared with summer, winter body temperature patterns were characterized by an absence of selective brain cooling (SBC), a higher range of T brain , a range of T carotid that was significantly narrower (1.8°C) than in summer (3.1°C), and changes in T carotid and T brain that were more highly correlated (r=0.99 in winter vs r=0.83 in summer). These findings suggest that in winter the effects of the carotid rete are reduced, which eliminates SBC and prevents independent regulation of T brain , thus coupling T brain to T carotid . The net effect is that T carotid varies little. A possible consequence is depression of metabolism, with the survival advantage of conservation of energy. These findings also suggest that the carotid rete has wider thermoregulatory effects than its traditional SBC function.

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We have found that pronghorn (Antilocapra americana) use external heat exchange with the environment and internal heat exchange between the carotid artery rete and cavernous venous sinus blood to regulate body temperature. Now we have investigated the relationship between the histological structure of the skin, cephalic veins, and carotid rete-cavernous sinus system and the physiological mechanisms pronghorn use, and whether their thermoregulatory anatomy has adaptive advantages. We harvested tissue samples of skin, three veins (i.e., angularis oculi vein, dorsal nasal vein, and facial vein), and the carotid rete-cavernous sinus system from four pronghorn, two culled in summer and two in winter, and examined each histologically. The three veins had the typical structure of veins with large lumina and thin walls. The carotid rete consisted of small (0.1-0.5 mm) arterioles with a density of~10/mm 2 , intertwined with veins (~2/ mm 2 ), enclosed within the cavernous sinus; a structure ideal for heat exchange. We concluded that the main function of the dorsal nasal and facial veins is to return cold blood to the body to effect whole body cooling. The cavernous sinus is supplied with warm blood by the palatine veins in winter and cold blood by the deep facial veins in summer, an arrangement different to that in other ungulates, such as sheep, in which the angularis oculi vein supplies the cavernous sinus. Pronghorn skin is richly supplied with blood vessels that facilitate convective heat loss in summer. In winter, the number of coarse and fine hairs per square millimeter increases more than in European deer to form a thick pelage that minimizes heat loss. In summer, the pelage is shed because hair follicles involute. Unlike in other ungulates, pronghorn skin has little adipose tissue. The number of apocrine glands increases in winter rather than in summer. We concluded that the glands have a reproductive/social function rather than a thermoregulatory one. In summary, our study shows that the thermoregulatory anatomy is consistent with our physiological data and has adaptive advantages that help explain the survival of pronghorn in an arid habitat characterized by extreme temperature variation and sparse vegetation.