_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 [.H]_{b} 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 T_{b}, 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 r_{max}.
_Bassariscus astutus_ is the only species with low [.H]_{b} 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 [.H]_{b}, 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 [.H]_{b}, improved insulative quality of
pelt, a more sharply defined molt cycle, improved capacity for
evaporative cooling, greater D_{d}, and higher r_{max}. Consequently,
by the upper Pliocene, two metabolically distinct groups of procyonids
could have been established: those species with low [.H]_{b} living in
climatically stable forests and those with higher [.H]_{b} living in
unstable tropical, subtropical, and perhaps temperate climates.
_Procyon lotor_ is the only extant procyonid with high [.H]_{b}.
_Procyon cancrivorus_ is its congeneric counterpart in Central and
South America (Table 1), and the two species are sympatric in Panama
and Costa Rica. However, in terms of its metabolism, thermal
conductance, molt, diversity of diet, r_{max}, and climatic
distribution, _Procyon cancrivorus_ shares more in common with other
procyonids than it does with _Procyon lotor_ (Tables 7, 11, 12; Figure
8). This suggests that metabolically _Procyon lotor_ portrays a
divergent line of this genus that arose as the result of a series of
mutations that gave rise to different metabolic characteristics. This
view is in keeping with a recent phylogenetic analysis of this family
that shows the genus _Procyon_ to be highly derived (Decker and
Wozencraft, 1991). Consequently, it would be instructive and would add
to our knowledge of the evolution of climatic adaptation to know more
about the genetic relatedness of these two species as well as their
historical relationship.
Genus _Procyon_ appears in the fossil record (Hemphillian and Blancan
ages; Baskin, 1982) prior to Pleistocene glaciations. During the
Pleistocene, there were four different glacial advances and retreats
in a relatively short time period (the first appearing little more
than a million years ago; Darlington, 1963:578-596; Webb, 1985a;
Marshall, 1988). Glacial retreats created pulses of time during which
subtropic and temperate climates advanced toward the poles into areas
with large seasonal differences in light/dark cycles, whereas glacial
advances pushed these climates southward into areas having smaller
seasonal differences in light/dark cycles (Raven and Axelrod, 1975;
Webb, 1977, 1978; Marshall, 1988). Those members of the genus
_Procyon_ caught in these wide latitudinal fluctuations would have
experienced conditions favorable to continued selection for
characteristics conducive to physiologic adaptation to a wide range of
climatic conditions. _Procyon lotor_ is the only member of its genus
to have survived this selective process, and as we have seen, it does
possess traits that adapt it to a wide range of climatic conditions.
Primary among these is its higher [.H]_{b}, which provides it with
advantages not shared with other procyonids (see earlier discussion).
Three other adaptations also have had a profound influence on _Procyon
lotor_'s ability to generalize its use of climate: (1) the increased
insulative quality of its pelt coupled with its sharply defined molt
cycle, which allows for a large annual change in thermal conductance;
(2) its annual cycle of fat storage; and (3) a diverse high-quality
diet. The first two of these adaptations required evolution of
neuroendocrine pathways capable of responding to time-dependent
environmental cues such as changing day length, changing temperature,
etc. Such conditions would have been available as selective stimuli in
high-latitude forests and savannas of interglacial periods. _Procyon
lotor_'s elevated basal metabolic rate would have increased its
overall energy requirement, and it makes good intuitive sense,
therefore, that evolution during the Pleistocene also would have
favored selection of a diverse diet containing many items of high
nutritive value.