Phylogenetic Influence on Primate Metabolic Variation

In addition to proximate ecological factors, phylogenetic inertia has been suggested as an explanation for hypometabolism in strepsirrhines and other mammal groups (e.g., Eisentraut, 1961; Elgar and Harvey, 1987; Martin, 1989; Ross, 1992). This hypothesis suggests that hypometabolism is a primitive mammalian trait that has been retained in extant strepsirrhines. While Kurland and Pearson (1986) discuss the possibility that strepsirrhines are hypometabolic because of phylogenetic inertia, they do not test this hypothesis. Ross (1992) lends some support to the role of phylogenetic effects on strepsirrhine hypometabolism, though problems with the methodology6 preclude acceptance of her results.

The results of the present study provide support for the phylogenetic inertia model, but an understanding of the metabolic rates of closely related species is important to test this hypothesis. The superorder Archonta was originally proposed by Gregory (1910) to contain primates, bats (order Chiroptera), colugos or "flying lemurs" (order Dermoptera), and the tree shrews and elephant shrews (order Menotyphla). McKenna (1975) later removed the elephant shrews leaving primates, colugos, bats, and tree shrews (order Scandentia) in the superorder. The superorder Archonta has been the subject of numerous investigations, using morphological studies of living species, paleontological studies, and molecular investigations (see review in Sargis, 2002). The validity of Archonta has received its greatest support from the result of comparative studies of skeletal characters of the ankle region (e.g., Szalay, 1977). However, testing the integrity of Archonta is problematic because of the dearth of fossil evidence in all but the primates. Additionally, the use of morphological traits that are primitive or convergent (rather than shared derived characters), has led to false support for Archonta (Martin, 1990).

No consensus exists on the integrity of Archonta as a monophyletic unit, but there are data both from morphological and molecular studies that support the close relationship of primates with other mammalian orders.

6 Ross (1992) compared metabolic data for primates with a regression generated by Stahl (1967). The Stahl regression is not based on 349 mammalian species, as claimed by Ross, but 349 data points. The paper does not provide information on which species were used and the number of data points for each and, additionally, does not control for animals in the resting condition. The scaling coefficient is higher and, consequently, Ross' calculations of metabolic deviations are invalid.

However, a number of recent studies have not supported Archonta as a monophyletic group, but instead support close relationships between subsets of the members. In particular, Euarchonta, which includes primates, colugos, and tree shrews (but not bats) has received support from molecular studies (Adkins and Honeycutt, 1991, 1993; Madsen et al., 2001; Murphy et al., 2001a,b; Stanhope et al., 1993), as well as combined morphological and molecular evidence (Liu and Miyamoto, 1999; Liu et al., 2001). Interestingly, some studies have indicated a close evolutionary relationship between Euarchonta and Glires (rodents and lagomorphs), together forming Euarchontoglires (Madsen et al., 2001; Murphy et al., 2001a,b).

Metabolic data for members of the superorder Archonta were available for tree shrews and bats. Unfortunately, no metabolic data are available for colugos. Both tree shrews and bats have, on average, lower metabolic rates than similar-sized mammals according to the Kleiber scaling relationship. In the two studies of RMR in tree shrews that were conducted under standardized conditions, both species measured were shown to be hypometa-bolic. Ptilocercus lowii, a nocturnal and arboreal tree shrew species, has an RMR 39.1% below that predicted by the Kleiber equation. Tupaia glis, which is diurnal and partially terrestrial (Martin, 1990; Nowak, 1991), is also hypometabolic and has an RMR 25.5% below that predicted by Kleiber scaling relationship. Both species are omnivorous and include various amounts of insects and fruits as the main items in their diet (Martin, 1990). Tree shrews have often been used as models of early primate morphology and behavior (and were classified by some authorities [e.g., Simpson, 1945] at one time as members of the primate order), largely because of their inferred close phylogenetic relationship and certain morphological similarities shared with primates. However, there is a good deal of morphological and behavioral variation between species of tree shrew, and many of the shared morphological traits may actually be either primitive or convergent (Martin, 1990). That said, there are indications from both molecular and morphological studies that Scandentia is closely related to primates, possibly as a sister group.

Bats have metabolic rates that average 10% below those predicted by the Kleiber equation, though this average masks considerable variation found within the order. While bats have metabolic rates lower than expected, they are not hypometabolic by previously described criteria. The scaling relationship between RMR and body mass in bats is: RMR = 53.5M071. Microbats

(n = 34) have metabolic rates nearly identical to megabats (family Pteropodidae; n = 12) and a similar range of variation in body size is seen in the two groups. Microbats on average deviate from that predicted by the Kleiber equation by -10%, whereas megabats deviate by on average -9%. Despite these low-metabolic rates, bats have the highest capacity gas exchange system found in living mammals (Szewczak, 1997).

The phylogenetic position of tarsiers among primates makes them an important group to examine in the phylogenetic argument since they possess numerous primitive mammalian traits that were subsequently lost in anthropoids (Martin, 1990). Molecular studies, using protein and DNA sequence evidence (Bonner et al., 1980; DeJong and Goodman, 1988; Dijan and Green, 1991; Koop et al., 1989a,b; Miyamoto and Goodman, 1990; Pollock and Mullin, 1987; Porter et al., 1995; Shoshani et al., 1996; Zietkiewicz et al., 1999), lend support to the classification of tarsiers as a sister clade of the anthropoids, both subsumed within the suborder Haplorhini. Additionally, many morphological studies based on derived features support the grouping of tarsiers as haplorhines (Beard et al., 1991; Martin, 1990; Ross, 1994; Szalay et al., 1987).

The only tarsier species with available metabolic measurements taken under standardized conditions is Tarsius syrichta, which has an RMR well below (-34.8%) that predicted by the Kleiber equation. Tarsiers are nocturnal, arboreal, and small-bodied, and the only primates that consume 100% animal material (mostly insects and some vertebrates). The depressed metabolic rates of tarsiers may be the result of the retention of a primitive mammalian trait, as is hypothesized for the strepsirrhines.

Taken as whole, metabolic rates in the closest living relatives of primates provide some evidence for hypometabolism as a primitive trait that has been retained in living strepsirrhines. However, further resolution of primate superordinal relationships, as well as further studies of metabolism in close relatives, are needed.

The phylogenetic explanation is often used as an unenlightening nonexpla-nation (e.g., Hayssen and Lacy, 1985), but in order to fully understand phy-logenetic inertia as an explanation, the reasons for the evolution of hypometabolism must be addressed. Additional questions that must be addressed are why hypometabolism was maintained in descendant lineages and whether there was active selection to maintain it in the extant species, or whether it was retained because there was not active selection against it.

Unfortunately, it is often difficult to unravel the effects of phylogeny from current adaptations, since phylogenetically close animals also tend to have similarities in both ecology and biology (Elgar and Harvey, 1987; McNab, 1986).

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