Trends in Genetics
Volume 26, Issue 8, August 2010, Pages 353-362
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Review
Evolutionary genetics in wild primates: combining genetic approaches with field studies of natural populations

https://doi.org/10.1016/j.tig.2010.05.005Get rights and content

Ecological and evolutionary studies of wild primates hold important keys to understanding both the shared characteristics of primate biology and the genetic and phenotypic differences that make specific lineages, including our own, unique. Although complementary genetic research on nonhuman primates has long been of interest, recent technological and methodological advances now enable functional and population genetic studies in an unprecedented manner. In the past several years, novel genetic data sets have revealed new information about the demographic history of primate populations and the genetics of adaptively important traits. In combination with the rich history of behavioral, ecological, and physiological work on natural primate populations, genetic approaches promise to provide a compelling picture of primate evolution in the past and in the present day.

Section snippets

Genetic studies of natural primate populations

Our closest living relatives, the nonhuman primates, are perennial subjects of public and scientific fascination because they occupy a unique place in evolutionary biology and ecology. The striking similarities we share with other primates make them important models for human physiology, behavior, and health 1, 2, 3, 4. At the same time, variation among primate populations and species provides a rich basis for comparative work (e.g. Refs 5, 6, 7). Such work is crucial for understanding the

Population structure and gene flow in a behavioral and ecological context

A central project of evolutionary geneticists focuses on understanding population history and demography. These are in turn mediated by individual dispersal patterns and differential reproductive success – parameters that have also been of great interest to primate field researchers. In particular, research on natural primate populations has focused intensively on the behavioral and ecological factors that contribute to variation in these characteristics (e.g. Refs 14, 15, 16). Placing genetic

Testing the selective import of functional variation

The action of natural selection on functional genetic variants (i.e. polymorphisms that have a causal relationship with trait variation) is responsible for much of the phenotypic diversity in behavior, physiology, and morphology exhibited by primates, including traits that differentiate humans from other primates. Identifying loci that have been targets of natural selection via sequence analysis is therefore a vital area of research in primate genetics. However, even when a locus is strongly

Functional genetics and the genotype–phenotype relationship in wild primates

One of the most exciting possibilities for genetic research in natural primate populations lies in the prospect of identifying functional genetic variation that influences ecologically and adaptively relevant traits (Box 3). This area of research is in the early phase of development. Indeed, the genome-scale approaches that will probably move this area forward have, until recently, been impracticable in wild primates. Thus, functional studies in primates have largely relied on candidate gene

What lies ahead for the genetics of natural primate populations?

Field-based ecological, behavioral, and demographic data already play an important role in genetic studies of nonhuman primates, and will be increasingly important in the future as the scope and scale of genetic data on wild primates grow. Recent technological and methodological advances, especially high-throughput sequencing approaches, represent a major advance for the field. Indeed, the extensive data collection these tools enable mean that, for the first time, the quality and quantity of

Novel data sets for resource development and genomic exploration.

As a direct consequence of the falling cost of genomic technologies, population-based data collection is becoming increasingly feasible to conduct, even for non-model organisms. As a result, individual investigators are now able to collect large genetic data sets tailored to their specific species and/or study populations, at a much more rapid rate than in the past. This development will not only lead to a vast increase in the availability of genetic markers, but will also allow primate

Population history and demography

Previous studies have provided important insights into demographic processes such as admixture and gene flow [18]. New waves of genetic data are positioned to build on this work by providing much more fine-grained estimates of these processes. These results will eventually allow us to investigate, for example, how and why the evolutionary histories of species that experienced similar patterns of historic environmental change might have differed. Genetic data can also be combined with

Functional genetics and the genotype–phenotype relationship

Trait-mapping studies will also be able to take advantage of larger-scale genotyping and resequencing data sets. For candidate gene studies, these approaches will provide much improved ability to correct for potential confounds, such as cryptic population structure and relatedness. Even more importantly, they will allow the field to expand its perspective beyond candidate genes to investigate previously uncharacterized loci. These studies will help address, for instance, the degree to which

Challenges

A central theme of this review is to emphasize how new technological and methodological developments are making it increasingly possible to conduct genetic studies in natural primate populations, where genetic inferences can be combined with behavioral, ecological, and other sources of data. Although these developments are unquestionably expanding the possibilities for research in primate genetics, some important challenges remain.

First, and especially for collection of genomic data sets other

Conclusions

Genetic studies in primates present the exciting possibility that genetic inferences can be placed in the context of complementary behavioral and ecological data about the same systems, gathered under natural conditions. This opportunity has been made possible by generations of primate field research. These efforts have produced a well-developed framework for understanding the causes and consequences of genetic evolution. As genomic resources for these species proliferate, natural primate

Acknowledgments

We thank G.H. Perry for directing us to some relevant pieces of literature and C.C. Babbitt and four anonymous reviewers for helpful comments on the manuscript. J.T. is supported by a Duke University Katherine Goodman Stern Dissertation Fellowship; S.C.A. is supported by National Science Foundation (NSF) grants DEB-0846286 and IOS-0919200 and National Institutes of Health (NIH) grants AG034513-01 and AG031719-01A1; G.A.W. is supported by NSF grants DEB-0846286 and BCS-0827552 and NIH grant

References (115)

  • S. Manel

    Landscape genetics: combining landscape ecology and population genetics

    Trends Ecol. Evol.

    (2003)
  • P.O. Onyango

    Persistence of maternal effects in baboons: mother's dominance rank at son's conception predicts stress hormone levels in subadult males

    Horm. Behav.

    (2008)
  • T.J. Roseboom

    Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview

    Mol. Cell. Endocrinol.

    (2001)
  • M.L. Arnold et al.

    Natural hybridization in primates: one evolutionary mechanism

    Zoology

    (2006)
  • C.A. Buerkle et al.

    Admixture as the basis for genetic mapping

    Trends Ecol. Evol.

    (2008)
  • J. Rogers

    An initial genetic linkage map of the rhesus macaque (Macaca mulatta) genome using human microsatellite loci

    Genomics

    (2006)
  • J. Rogers

    A genetic linkage map of the baboon (Papio hamadryas) genome based on human microsatellite polymorphisms

    Genomics

    (2000)
  • J.C. Mitani et al.

    Why do chimpanzees hunt and share meat?

    Anim. Behav.

    (2001)
  • C.S. Barr

    The utility of the non-human primate model for studying gene by environment interactions in behavioral research

    Genes Brain Behav.

    (2003)
  • F.L. Bellino et al.

    Nonhuman Primate Models of Menopause Workshop

    Biol. Reprod.

    (2003)
  • C.J. Jolly

    A proper study for mankind: analogies from the papionin monkeys and their implications for human evolution

    Yearb. Phys. Anthropol.

    (2001)
  • A.M. Bronikowski

    The aging baboon: comparative demography in a non-human primate

    Proc. Natl. Acad. Sci. U. S. A.

    (2002)
  • C.L. Nunn

    Promiscuity and the primate immune system

    Science

    (2000)
  • C.P. Van Schaik et al.

    Infanticide risk and the evolution of male–female association in primates

    Proc. R. Soc. Lond. B Biol. Sci.

    (1997)
  • A. Di Fiore et al.

    Molecular primatology

  • A. Siepel

    Phylogenomics of primates and their ancestral populations

    Genome Res.

    (2009)
  • J.C. Buchan

    True paternal care in a multi-male primate society

    Nature

    (2003)
  • L. Vigilant

    Paternity and relatedness in wild chimpanzee communities

    Proc. Natl. Acad. Sci. U. S. A.

    (2001)
  • S.C. Alberts et al.

    Balancing costs and opportunities: dispersal in male baboons

    Amer. Nat.

    (1995)
  • D.L. Cheney

    Reproductive success in vervet monkeys

  • R.R. Lawler

    Fitness and extra-group reproduction in male Verreaux's sifaka: an analysis of reproductive success from 1989–1999

    Am. J. Phys. Anthropol.

    (2007)
  • L. Vigilant

    Elucidating population histories using genomic DNA sequences

    Curr. Anthropol.

    (2009)
  • R.K. Chesser

    Influence of gene flow and breeding tactics on gene diversity within populations

    Genetics

    (1991)
  • E.A. Archie

    Fine-scale population genetic structure in a fission–fusion society

    Mol. Ecol.

    (2008)
  • K. Foerster

    A spatial genetic structure and effects of relatedness on mate choice in a wild bird population

    Mol. Ecol.

    (2006)
  • D.H. Nussey

    Rapidly declining fine-scale spatial genetic structure in female red deer

    Mol. Ecol.

    (2005)
  • J. Altmann

    Behavior predicts genetic structure in a wild primate group

    Proc. Natl. Acad. Sci. U. S. A.

    (1996)
  • T.R. Pope

    The influence of dispersal patterns and mating system on genetic differentiation within and between populations of the red howler monkey (Alouatta seniculus)

    Evolution

    (1992)
  • C.P. Van Schaik

    The ecology of social relationships amongst female primates

  • R.W. Wrangham

    An ecological model of female-bonded primate groups

    Behaviour

    (1980)
  • R.R. Ackermann et al.

    Morphological and molecular evidence reveals recent hybridization between gorilla taxa

    Evolution

    (2010)
  • O.H. Thalmann

    The complex evolutionary history of gorillas: insights from genomic data

    Mol. Biol. Evol.

    (2007)
  • C. Becquet

    Genetic structure of chimpanzee populations

    PLoS Genet.

    (2007)
  • J.L. Caswell

    Analysis of chimpanzee history based on genome sequence alignments

    PLoS Genet.

    (2008)
  • R.D. Hernandez

    Demographic histories and patterns of linkage disequilibrium in Chinese and Indian rhesus macaques

    Science

    (2007)
  • M.J.E. Charpentier

    Age at maturity in wild baboons: genetic, environmental and demographic influences

    Mol. Ecol.

    (2008)
  • J. Tung

    Genetic evidence reveals temporal change in hybridization patterns in a wild baboon population

    Mol. Ecol.

    (2008)
  • N.J. Dominy et al.

    Ecological importance of trichromatic vision to primates

    Nature

    (2001)
  • J.D. Mollon

    Tho she kneel’d in that place where they grew …” The uses and origins of primate colour vision

    J. Exp. Biol.

    (1989)
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    Present address: Department of Human Genetics, University of Chicago, 920 E 58th Street, Chicago, IL 60637, USA.

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