Genetic studies on the Cayo Santiago rhesus macaques: A review of 40 years of research

Abstract

Genetic studies not only contribute substantially to our current understanding of the natural variation in behavior and health in many species, they also provide the basis of numerous in vivo models of human traits. Despite the many challenges posed by the high level of biological and social complexity, a long lifespan and difficult access in the field, genetic studies of primates are particularly rewarding because of the close evolutionary relatedness of these species to humans. The free-ranging rhesus macaque (Macaca mulatta) population on Cayo Santiago (CS), Puerto Rico, provides a unique resource in this respect because several of the abovementioned caveats are of either minor importance there, or lacking altogether, thereby allowing long-term genetic research in a primate population under constant surveillance since 1956. This review summarizes more than 40 years of genetic research carried out on CS, from early blood group typing and the genetic characterization of skeletal material via population-wide paternity testing with DNA fingerprints and short tandem repeats (STRs) to the analysis of the highly polymorphic DQB1 locus within the major histocompatibility complex (MHC). The results of the paternity studies also facilitated subsequent studies of male dominance and other factors influencing male reproductive success, of male reproductive skew, paternal kin bias, and mechanisms of paternal kin recognition. More recently, the CS macaques have been the subjects of functional genetic and gene expression analyses and have played an important role in behavioral and quantitative genetic studies. In addition, the CS colony has been used as a natural model for human adult-onset macular degeneration, glaucoma, and circadian rhythm disorder. Our review finishes off with a discussion of potential future directions of research on CS, including the transition from STRs to single nucleotide polymorphism (SNP) typing and whole genome sequencing.

A 75‐year pictorial history of the Cayo Santiago rhesus monkey colony

“…Once caught, they are sedated and yearlings are tattooed and ear notched. In recent years, yearlings and other animals have been given physical examinations, provided biological samples for studies, and bled for paternity testing and maternity confirmation using genetic analyses [see Widdig et al, 2015, this issue].…”

“…The collection now consists of over 3,600 complete boxed rhesus skeletons, including 3,000 from CS rhesus (Fig. 51) [Dunbar, 2012; Wang, 2012, 2015, this issue; Widdig et al, 2015, this issue].…”

“…A total of 600 animals were removed representing about half of the population. Group M has been kept at SSFS for the past 30 years for a variety of behavioral and biomedical research not feasible on CS [for reviews, see Widdig et al, 2015, this issue; Zhdanova et al, 2015, this issue]. After the cull was completed, Figueroa retired and Davila replaced him as chief census taker, a position that he still holds.…”

“…CPRC management and research programs became a national model for collaborative investigations involving both field and laboratory studies putting the CPRC in the forefront of primate research into genetics; demography; comparative diseases of aging (arthritis, osteoporosis, spondyloarthropathy, diabetes, glaucoma and macular degeneration); socioendocrinology, sociobiology and neurobiology; cognition and communicative behavior; and reproductive biology and embryology. His continued support of the CPRC Skeletal Collection allowed it to expand and become one of the world's most important research resources for osteological investigations on skeletal biology and disease, especially because of its accompanying genetic and life history databases [Dunbar, 2012; Wang, 2012; Widdig et al, 2015, this issue].…”

“…This led to a long-term collaboration with Joerg Schmitdke and his genetic group at the Institute of Human Genetics in Hannover beginning with Berard's studies on the life histories of CS males [Berard et al, 1993]. The collaboration has grown over the years, now encompassing several institutions, and has resulted in numerous publications [for a review, see Widdig et al, 2015, this issue].…”