Evolution of Metabolic Adaptations
Evolution of Low Basal Metabolic Rate
A radiation of frugivorous and omnivorous Procyoninae ([Table 1]) occurred in the middle and late Miocene of North America. It included origins of such terrestrial genera as Cyonasua, Nasua, and Procyon (Webb, 1985b). The earliest procyonid genus to find its way to South America was Cyonasua, an omnivorous carnivore that presumably split, along with its sister genus Arctonasua, from a common North American ancestor (Baskin, 1982; Webb, 1985b). Cyonasua, about the size of present-day raccoons, was adapted to a wide range of habitats and was probably comparable to modern raccoons with respect to the breadth of its feeding habits (Webb, 1985b; Marshall, 1988). Because North American Arctonasua was about the same size as Cyonasua (Webb, 1985b) and shared a number of characters with it (Baskin, 1982), we speculate that it also may have had similar habits and occupied similar climates and habitats. Bassariscus, another member of Procyoninae, had an even earlier origin in tropical North America (Webb, 1985b). The origin of the small arboreal forms Potos and Bassaricyon (subfamily Potosinae) is obscure but is thought to have occurred in the rainforests of Central America (Webb, 1985b). What were the metabolic capabilities of these early procyonids? We do not know, but for several million years, from middle to late Miocene, procyonids lived in tropical and subtropical forests of Central and North America (Webb, 1985b; Marshall, 1988). Then, in the Pleistocene, several modern forms crossed the Panamanian land bridge into similar habitats and climates in South America; but none of them appear to have spread far enough northward to have crossed the Bering land bridge.
Several million years exposure to a tropical environment, with its continuous high temperatures and modest range of thermal extremes, would have favored selection of metabolic and thermoregulatory traits that would minimize energy requirements: a lower than predicted basal metabolic rate, a prolonged or continuous molt resulting in very little annual change in minimum thermal conductance, and a modest capacity for evaporative cooling. In addition, we would expect selection to have favored a diverse diet, good reproductive potential, and behavioral flexibility to utilize a variety of habitats within these climates. Our analysis has shown that such characteristics are the norm for extant members of this family living in tropical and subtropical climates, and we speculate that these traits also were common to early procyonids and served to restrict them to these climates. Our speculation is supported by the fact that their known fossil history from the Miocene is confined to geographic areas that had tropical and subtropical climates.
Later on, during Pleistocene glaciations, tropical and subtropical forests shrank, savannas expanded, and temperate climate was pushed toward equatorial regions. The opposite occurred during interglacial periods (Raven and Axelrod, 1975; Webb, 1977, 1978; Marshall, 1988). Consequently, mid-latitudes experienced alternating periods of temperate and tropical, or at least subtropical, climate change. Selection of characteristics that would have adapted a species with low Ḣb to temperate as well as tropic or subtropic climates could have occurred in mid-latitudes at the temperate edge of these tropical advances and retreats. Our analysis indicates that, for this purpose, selection would have favored lower than predicted thermal conductance, seasonal molt, increased capacity for evaporative cooling, increased tolerance of elevated Tb, increased flexibility of thermoregulatory behavior, food habits that provided for year-round access to a high-quality diet in all three climates, and a higher than predicted rmax.
Bassariscus astutus is the only species with low Ḣb that has all these characteristics, and it is the only one of them that has added temperate climate to its distribution ([Table 11]). This suggests that Bassariscus astutus is a species that evolved away from the norm for procyonids with low Ḣb, toward characteristics that allowed it to become more of a climate generalist. Potos flavus, with its dietary specialization, low tolerance to high temperatures, and arboreal mode of existence, has become a highly specialized species totally dependent on tropical forests for its survival. As such, it also represents a species that has evolved away from the procyonid norm and portrays the extreme in climate specialization. Olingos, Bassaricyon gabbii ([Table 1]), may be similar to Potos flavus in this respect (see also [Table 10]). This suggests that of the extant procyonids, Nasua nasua, Nasua narica, and Procyon cancrivorus have retained metabolic and behavioral characteristics that are closest to those of their Miocene ancestors.
Evolution of High Basal Metabolic Rate
Between the time that Cyonasua appeared and the Panamanian land bridge was established in the upper Pliocene (4 to 5 million years ago), northern climates continued their gradual cooling. This, along with ongoing elevation of the continents and continuous modification of their mountain ranges, served to shrink the tropical forest and create pockets of climatic instability within it and on its edges (Darlington, 1963:578-596; Marshall, 1988). In areas of instability, selection would have favored traits that provided for a broader range of thermal tolerance: higher Ḣb, improved insulative quality of pelt, a more sharply defined molt cycle, improved capacity for evaporative cooling, greater Dd, and higher rmax. Consequently, by the upper Pliocene, two metabolically distinct groups of procyonids could have been established: those species with low Ḣb living in climatically stable forests and those with higher Ḣb living in unstable tropical, subtropical, and perhaps temperate climates.