Answer: Nonhuman primate (NHP) aging research has traditionally relied mainly on the rhesus macaque. But the long lifespan, low reproductive rate, and relatively large body size of macaques and related Old World monkeys make them less than ideal models for aging research. Manifold advantages would attend the use of smaller, more rapidly developing, shorter-lived NHP species in aging studies, not the least of which are lower cost and the ability to do shorter research projects. Arbitrarily defining “small” primates as those weighing less than 500 g, we assess small, relatively short-lived species among the prosimians and callitrichids for suitability as models for human aging research. Using the criteria of availability, knowledge about (and ease of) maintenance, the possibility of genetic manipulation (a hallmark of 21st century biology), and similarities to humans in the physiology of age-related changes, we suggest three species—two prosimians (Microcebus murinus and Galago senegalensis) and one New World monkey (Callithrix jacchus)—that deserve scrutiny for development as major NHP models for aging studies. We discuss one other New World monkey group, Cebus spp., that might also be an effective NHP model of aging as these species are longer-lived for their body size than any primate except humans.
Keywords: aging, bush baby (Galago senegalensis), lemur (Microcebus murinus), longevity, marmoset (Callithrix jacchus), nonhuman primate (NHP), prosimian, tamarin (Saguinus spp.)
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Introduction: Considerations for Species Selection in Aging Research
Mice and Rats
The standard mammalian models used in biomedical research are murine rodents, and from a practical perspective there are many research advantages to mice and rats: they are relatively short-lived and inexpensive to house; their genetics, biology, and husbandry are tractable and well understood; and they are early and copious breeders, making them useful, practical, and economical for many different research applications. Moreover, mice in particular have very tractable genetics, allowing specific genes to be turned off or overexpressed ubiquitously or only in specific tissues under specific conditions (more on genetic manipulation below).
But rodents are only distantly related to humans, having diverged some 84–121 million years ago (Glazko et al. 2005), and the very characteristics that make them easy to keep in the laboratory also distinguish their life histories from those of humans in important ways. Because rodents lead relatively fast (r-selected) lives, with low survivorship and strong selection for early and copious reproduction, there are likely to be significant differences in the biology of rodent and human aging. For instance, mice and rats experience estrus rather than menstrual cycles and so make poor models for reproductive aging (Black and Lane 2002). Similarly, mice do not suffer from atherosclerosis and other cardiovascular diseases that are important causes of morbidity and mortality among humans, and the profile of tumors they contract spontaneously is very different from that of humans (Waters and Wildasin 2006). Finally, with life histories at the opposite end of the fast-slow continuum, the evolutionary pressures that have shaped aging, such as selection of pleiotropic effects, may differ significantly between humans and rodents.
Nonhuman Primates
Animals share two kinds of traits: (1) morphological and functional characteristics that are conserved across a wide range of distantly related species (e.g., the impact of insulin/IGF [insulinlike growth factor] signaling on longevity in worms, flies, and mice; Tatar et al. 2003) and (2) idiosyncratic traits that are either shared only between more closely related species (e.g., menstrual cycles in Old World primates; Kaplan and Manuck 2008; Martin et al. 2003) or confined to a single species (e.g., Alzheimer’s disease in humans; Finch and Sapolsky 1999). Because of their close phylogenetic relationship with humans, primates share a large number of both types of traits important in human aging. They also have a characteristically slow (K-selected) life history, with relatively high survivorship, delayed breeding, long inter-birth interval, and low reproductive output similar to humans. Shared life history characteristics reflect similar selective forces and constraints, which shape aging in both humans and nonhuman primates (NHP1). Nonhuman primates therefore offer a logical model for age-related research and preclinical testing of aging interventions.
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