Heritability of Fearful-Anxious Endophenotypes in
Infant Rhesus Macaques: A Preliminary Report
Douglas E. Williamson, Kris Coleman, Silviu-Alin Bacanu, Bernie J. Devlin,
Jeffrey Rogers, Neal D. Ryan, and Judy L. Cameron
Background: Research efforts to discover the genetic
underpinnings of anxiety and depression is challenging
because of the etiologic heterogeneity inherent to these
disorders. These efforts might be aided by the study of
related behavioral phenotypes in model organisms, such
as monkeys.
Methods: Eighty-five rhesus monkeys (Macaca mulatta)
from the Oregon National Primate Research Center were
drawn from a standard matriarchal colony and tested for
behavioral response in four testing paradigms designed to
elicit fearful-anxious reactions. Heritabilities were esti-
mated using variance component-based quantitative ge-
netic analyses with much of the genetic information
arising from paternal half-sibs.
Results: Individual behaviors reflecting increased distress
responses (e.g., vocalizations and teeth grinding) and
behavioral inhibition (e.g., latency to leave mother, la-
tency to inspect novel fruit) showed significant heritability,
even though a small number of monkeys were assessed.
Exploratory factor analyses identified seven clusters of
behaviors across tests, some of which were found to be
heritable.
Conclusions: These results indicate that several specific
fearful-anxious behaviors in infant rhesus monkeys are
heritable within this colony. Accordingly, these pheno-
types, which are believed to represent the genetic liability
for anxiety and depression, are good candidates for
further genetic investigation in this population. Biol
Psychiatry 2003;53:284 –291 © 2003 Society of Biologi-
cal Psychiatry
Key Words: Endophenotypes, heritability, model organ-
isms, anxiety, depression
Introduction
A
nxiety and depressive disorders are strongly familial,
especially those beginning in childhood or early
adulthood (Kovacs and Devlin 1998; Moldin et al 1991;
Williamson et al 1995, 1999). The younger the age of the
affected proband, the greater the hazard for the disorder in
family members (Kupfer et al 1989; Neuman et al 1997;
Weissman et al 1988; Williamson et al 1995), suggesting
that early onset may represent a highly genetic form of the
disease. Anxiety and depressive disorders are comorbid
and co-occur within families (Angold and Costello 1993;
Kovacs et al 1989; Ryan et al 1987; Williamson et al,
1999). As reviewed by Kovacs and Devlin (1998), adop-
tion, twin, and family studies suggest that both kinds of
illness have a genetic basis and that the same genes can
affect liability to both kinds of disorders (e.g., Kendler et
al 1987, 1992, 1993, 1995; Williamson et al 1999);
however, despite the mounting evidence suggesting that
these two common, intertwined psychiatric illnesses have
a substantial genetic component, it could still be difficult
to identify these genetic causes, as has proven true for
similarly complex diseases (Risch 2000).
Heterogeneity of the anxiety and depression phenotypes
argues for careful consideration of designs for genetic
analysis. One possibly efficacious strategy is to study traits
that predate the onset of the disorders or are strongly
associated with disease. Furthermore, these traits should
be assessable in all family members regardless of the
degree to which they are affected. Although not a panacea,
such strategies have the potential to increase the power of
the analysis (Blangero et al 2000). For early-onset anxiety
and depression, such traits or “endophenotypes” could
include putative biological markers such as growth hor-
mone response to challenge, which has been shown to be
blunted in depressed children (Dahl et al 2000), children at
high risk for depression (Birmaher et al 2000), as well as
adults with anxiety disorders (Price et al 1995; Uhde
1986). Another potentially fruitful approach involves
studying behavioral traits that are believed to underlie the
risk for developing anxiety or depression. For example,
temperamental characteristics reflecting behavioral inhibi-
From the Department of Psychiatry (DEW, KC, S-AB, BJD, NDR, JLC), Univer-
sity of Pittsburgh Medical Center, Western Psychiatric Institute and Clinic,
Pittsburgh, Pennsylvania; Oregon National Primate Research Center (KC,
JLC), Beaverton, Oregon; Southwest National Primate Research Center (JR),
San Antonio, Texas.
Address reprint requests to Douglas E. Williamson, Ph.D., Department of Psychi-
atry, University of Pittsburgh School of Medicine, Room E-723, Western
Psychiatric Institute and Clinic, 3811 O’Hara Street, Pittsburgh PA 15213.
Received May 13, 2002; revised July 29, 2002; accepted August 1, 2002.
© 2003 Society of Biological Psychiatry 0006-3223/03/$30.00
PII S0006-3223(03)01601-3