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Reactive heritability of extraversion: Where do we stand?

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Abstract

Researchers have puzzled over the " missing heritability " problem for quantitative traits, including personality dimensions such as the Big Five. Specifically, although all human personality traits exhibit substantial additive genetic variance, large gene association studies with immense statistical power have failed to discover specific genes that explain even a fraction of this estimated heritability (e.g., Service, Verweij, Lahti, Congdon, et al., 2012). Because such effects are prerequisite for the maintenance of personality differences via fluctuating (including frequency-dependent) selection on specific polymorphic genotypes, this initially promising type of evolutionary genetic model would seem to be rendered untenable by the empirical data as an explanation for the heritability of personality (Lukaszewski & von Rueden, 2015; Verweij et al., 2012). Recently, Lukaszewski and Roney (2011) hypothesized that part of extraversion's genetic variance reflects its facultative calibration to highly heritable, condition-dependent phenotypic features that would have predicted the cost–benefit ratio of extraverted strategies across ancestral environments. Specifically, we predicted that extraversion would have been a more beneficial strategy on average for more physically attractive and stronger individuals. If strength and attractiveness are in turn heritable due to genetic effects on condition — for instance, individuals with lower mutation loads develop both stronger and more attractive phenotypes — then extraversion would be heritable even if no specific genes directly encode for it. Such " reactive heritabil-ity " (see Tooby & Cosmides, 1990), if confirmed, could provide both a partial explanation for the missing heritability problem and a functional explanation for why individuals differ in extraversion. In prima facie support of the reactive heritability hypothesis, multiple empirical studies have found that measures of physical strength and attractiveness, respectively, positively predict individual differences in extraversion and related interpersonal dimensions (for a review of these findings, see Lukaszewski & Roney, 2011; Lukaszewski & von Rueden, 2015). As such, we have advocated for quantitative genetic studies to provide a proper test of extraversion's reactive heritability. In the current issue of Evolution and Human Behavior, Haysom et al. (2015) report a quantitative genetic test of the hypothesis that extra-version exhibits reactive heritability in relation to condition-dependent phenotypic features. Using a classical twin study design, they tested for phenotypic and genetic correlations of extraversion with other-rated facial attractiveness (from headshot photos), body mass index (BMI), height (as a proxy for strength) and intelligence test scores. Overall, results were not very supportive of the reactive heritability hypothesis: Of the phenotypic features examined , only facial attractiveness exhibited the predicted positive association with extraversion, and this effect explained at most a few percent of extraversion's additive genetic variance. Haysom et al. concluded that their findings cast some doubt on the viability of the reactive heritability hypothesis of extraversion. We do not entirely disagree. This was in some ways the most sophisticated test of the reactive heritability hypothesis ever conducted, and it appears to indicate that putative measures of condition-dependent phe-notypic features collectively explain very little of the heritable variance in extraversion. At the very least, then, this study reports empirical patterns that must be accounted for. However, we believe that the Haysom et al. study is inconclusive as a falsification of the reactive heritability hypothesis in light of several substantive (but understandable) limitations. Most importantly, the operational definitions of condition-dependent features employed in this study do not compellingly tap the most theoretically relevant aspects of strength, intelligence, and attractiveness: i. Height is only weakly-to-moderately correlated with physical strength. In our own data sets, measured upper-body strength has shown robust positive correlation with extraversion and related traits in both college undergraduates (Lukaszewski, 2013; Lukaszewski & Roney, 2011) and Amazonian forager–horticulturalists (von Rueden, Lukaszewski, & Gurven, 2015). However, height is much more weakly (and non-significantly) associated with extraversion in these same data sets. Therefore, a direct measure of physical strength might well have produced different results that increased the collective contribution of condition-dependent features to extraversion's genetic variance. ii. We do not doubt that intelligence test scores likely reflect mutation load and components of phenotypic condition, but we are not convinced that psychometric test performance would have been the most ancestrally predictive of one's ability to accrue benefits through extraverted strategies. Within small-scale societies, the most socially valued skills and abilities are often those that enhance one's capacity to manage coalitional alliances or excel in food production (von Rueden, Gurven, & Kaplan, 2008). Correspondingly , recent evidence suggests that the ability to detect and accommodate shifting contingencies is a narrow facet of intelligence that predicts peoples' effectiveness in accruing benefits via social exchange and competition — an effect that is not explained Evolution and Human Behavior xxx (2015) xxx–xxx
Commentary
Reactive heritability of extraversion: where do we stand?
Aaron W. Lukaszewski
a,
,JamesR.Roney
b
a
Department of Psychology, Oklahoma State University, Stillwater OK 74074
b
Department of Psychological and Brain Sciences, University of California, Santa Barbara
Researchers have puzzled over the missing heritabilityproblem
for quantitative traits, including personality dimensions such as the
Big Five. Specically, although all human personality traits exhibit sub-
stantial additive genetic variance, large gene association studies with
immense statistical power have failed to discover specic genes that ex-
plain evena fraction of this estimated heritability (e.g., Service, Verweij,
Lahti, Congdon, et al., 2012). Because such effects are prerequisite for
the maintenance of personality differences via uctuating (including
frequency-dependent) selection on specic polymorphic genotypes,
this initially promising type of evolutionary genetic model would
seem to be rendered untenable by the empirical data as an explanation
for the heritability of personality (Lukaszewski & von Rueden, 2015;
Verweij et al., 2012).
Recently, Lukaszewski and Roney (2011) hypothesized that part of
extraversion's genetic variance reects its facultative calibration to
highly heritable, condition-dependent phenotypic features that would
have predicted the costbenet ratio of extraverted strategies across
ancestral environments. Specically, we predicted that extraversion
would have been a more benecial strategy on average for more phys-
ically attractive and stronger individuals. If strength and attractiveness
are in turn heritable due to genetic effects on condition for instance,
individuals with lower mutation loads develop both stronger and
more attractive phenotypes then extraversion would be heritable
even if no specic genes directly encode for it. Such reactive heritabil-
ity(see Tooby & Cosmides, 1990), if conrmed, could provide both a
partial explanation for the missing heritability problem and a functional
explanation for why individuals differ in extraversion.
In prima facie support of the reactive heritability hypothesis, multi-
ple empirical studies have found that measures of physical strength
and attractiveness, respectively, positively predict individual differences
in extraversion and related interpersonal dimensions (for a review of
these ndings, see Lukaszewski & Roney, 2011; Lukaszewski & von
Rueden, 2015). As such, we have advocated for quantitative genetic
studies to provide a proper test of extraversion's reactive heritability.
In the current issue of Evolution and Human Behavior,Haysom et al.
(2015) report a quantitative genetic test of the hypothesis that extra-
version exhibits reactive heritability in relation to condition-
dependent phenotypic features. Using a classical twin study design,
they tested for phenotypic and genetic correlations of extraversion
with other-rated facial attractiveness (from headshot photos), body
mass index (BMI), heigh t (as a proxy f or streng th) and int elli-
gence test scores. Overall, results were not very supportive of
the reactive heritability hypothesis:Of thephenotypic featuresexam-
ined, only facial attractiveness exhibited the predicted positive association
with extraversion, and this effect explained at most a few percent of
extraversion's additive genetic variance.
Haysom et al. concluded that their ndings cast some doubt on the
viability of the reactive heritability hypothesis of extraversion. We do
not entirely disagree. This was in some ways the most sophisticated
test of the reactive heritability hypothesis ever conducted, and it ap-
pears to indicate that putative measures of condition-dependent phe-
notypic features collectively explain very little of the heritable
variance in extraversion. At the very least, then, this study reports em-
pirical patterns that must be accounted for.
However, we believe that the Haysom et al. study is inconclusiveas a
falsication of the reactive heritability hypothesis in light of several sub-
stantive (but understandable) limitations. Mostimportantly, the opera-
tional denitions of condition-dependent features employed in this
study do not compellingly tap the most theoretically relevant aspects
of strength, intelligence, and attractiveness:
i. Height is only weakly-to-moderately correlated with physical
strength. In our own data sets, measured upper-body strength has
shown robust positive correlation with extraversion and related traits
in both college undergraduates (Lukaszewski, 2013; Lukaszewski &
Roney, 2011)andAmazonianforagerhorticulturalists (von Rueden,
Lukaszewski, & Gurven, 2015). However, height is much more weak-
ly (and non-signicantly) associated with extraversion in these
same data sets. Therefore, a direct measure of physical strength
might well have produced different results thatincreased the col-
lective contribution of condition-dependent features to
extraversion's genetic variance.
ii. We do not doubt that intelligence test scores likely reect muta-
tion load and components of phenotypic condition, but we are
not convinced that psychometric test performance would have
been the most ancestrally predictive of one's ability to accrueben-
ets through extraverted strategies. Within small-scale societies,
the most socially valued skills and abilities are often those that en-
hance one's capacity to manage coalitional alliances or excel in
food production (von Rueden, Gurven, & Kaplan, 2008). Corre-
spondingly, recent evidence suggests that the ability to detect
and accommodate shifting contingencies is a narrow facet of intel-
ligence that predicts peoples' effectiveness in accruing benets via
social exchange and competition an effect that is not explained
Evolution and Human Behavior xxx (2015) xxxxxx
http://dx.doi.org/10.1016/j.evolhumbehav.2015.04.001
1090-5138/Published by Elsevier Inc.
Corresponding author. Tel.: +1 405 744 4277.
E-mail address: aaron.lukaszewski@okstate.edu (A.W. Lukaszewski).
Contents lists available at ScienceDirect
Evolution and Human Behavior
journal homepage: www.ehbonline.org
Please cite this article as: Lukaszewski, A.W., & Roney, J.R.,Reactive heritability of extraversion:where do we stand?, Evolution and Human Behav-
ior (2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.04.001
by general intelligence (Ronay & von Hippel, 2015). Thus, it re-
mains entirely possible that extraversion is in fact calibrated to
certain domain-specic mental abilities that are not tapped by
general intelligence batteries.
iii. Although other-rated facial attractiveness was (as in previous
studies) positively correlated with extraversion in both sexes,
these effects would likely have been larger if more complete infor-
mation regarding overall attractiveness were available in the stim-
uli. Facial attractiveness as rated from neutral headshots explains
part of the variance in overall attractiveness, but cues present in
the body, the voice, and patterns of dynamic motion explain a sub-
stantial amount of additional variance (e.g., Confer, Perilloux, &
Buss, 2010; Saxton, Burriss, Murray, Rowland, & Roberts, 2009).
This suggests that the true association of other-rated attractive-
ness with extraversion was likely underestimated when using
ratings of a single static headshot for each research subject. Con-
sistent with this, previousstudies that have employed composite
scores based on ratings of standardized total body photos have re-
ported attractivenessextraversion associations that are much
larger than those reported by Haysom et al. (e.g., Lukaszewski &
Roney, 2011).
iv. Finally, this study did not include self-perceptive measures of
strength, intelligence, or attractiveness. This is problematic
from our theoretical perspective, which posits that personality
strategies should be most directly calibrated to internal represen-
tations of one's relative bargaining power, which are computed
via comparisons of oneself with others on phenotypic dimen-
sions that inuence one's ability to confer benets or inict
costs on others (see Lukaszewski, 2013). Consistent with this,
(i) self-perceptions of condition-dependent phenotypic features
are more strongly and consistently associated with extraversion
than are more objectivemeasures and (ii) associations of
other-rated attractiveness and measured physical strength with
extraversion are mediated via self-perceptions (Lukaszewski,
2013; Lukaszewski & Roney, 2011).
The omission of self-perceptive measures of phenotypic features
could have produced particularly misleading results given that Haysom
et al. compared subjects sampled from different geographical regions
and time periods. Because these individuals did not come from the
same face-to-face populations, subjects' internal estimates of their
own bargaining power were presumably based on social comparisons
with essentially non-overlapping groups of other people. As such, this
could have resulted in comparing externally valid measures of individ-
uals' phenotypic features that do not closely correspond to their cue-
based internal representations (i.e. self-perceptions) that theoretically
drive personality calibration. These considerations imply that self-
perceptive measures of condition-dependent features, if included in
the study, would likely have exhibited robust positive associations
with extraversion.
In sum, a consideration of the limitations of the operational deni-
tions and sampling methods of Haysom et al.'s study supports the as-
sessment that it could have easily underestimated the true
magnitudes of the calibrational effects of condition-dependent pheno-
typic features on extraversion levels. In this context, we note that asso-
ciations of condition-dependent features with extraversion would not
need to be large in order to help solve important theoretical problems.
For example, condition-dependent reactive heritability could help eluci-
date why extraversion remains highly heritable within populations de-
spite its consistent positive association with tness-related outcomes
even if extraversion's calibration to all condition-dependent features
combined only explained a minority of its genetic variance on aver-
age. Thus, in evaluating this hypothesis, it is crucial for research to
employ theoretically appropriate measures and sampling tech-
niques that are able to detect even fairly small phenotypic and ge-
netic correlations.
Indeed, a recent study (von Rueden et al., 2015) lacks some of the
limitations of the Haysom et al. study and provides support for the reac-
tive heritability hypothesis. This investigation examined condition-
dependent phenotypic features in relation to personality in a large sam-
ple of Tsimane' foragerhorticulturalists indigenous to the Bolivian
Amazon. Most importantly, it was found that (i) measured upper-
body strength and the possession of locally valued knowledge, respec-
tively, exhibited independent positive associations with extraversion
and prosocial leadership orientation and (ii) controlling for physical
strength and locally valued knowledge signicantly reduced the esti-
mated heritability of these extraversion-related dimensions. Although
this study was limited in that its pedigree-based heritability estimates
do not fully control for possible effects of shared environment, it suc-
cessfully demonstrated that familial resemblance on extraversion-
related dimensions is explained in part by condition-dependent pheno-
typic features.
These two recent investigations (Haysom et al., 2015; von Rueden
et al., 2015) are the only two of which we are aware that directly test
for genetic correlations between condition-dependent features and ex-
traversion. Each ofthese studies contains a unique set of methodological
strengths and limitations, and they come to somewhat contradictory
conclusions. It will therefore be left to future research to arbitrate be-
tween them. Overall, we remain tentatively encouraged by the state of
the evidence in supporting the viability of the reactive heritability hy-
pothesis as applied to extraversion.
We will close by highlighting a humbling truth: Even under the best-
case scenario for our hypothesis wherein future studies nd compel-
ling support for extraversion's reactive heritability most of the genetic
variance in extraversion and all other human personality dimensions
would remain unexplained. The missing heritability problem thus per-
sists as a major unsolved mystery in behavioral and evolutionary genet-
ics. In a recent article, Lukaszewski and von Rueden (2015) reviewed
the state of the evidence and concluded that much of the genetic vari-
ance in personality likely reects noisy (i.e. directionally random) orga-
nizational effects of low frequency genotypes maintained in the context
of mutation-selection balance and pathogenhost coevolution (see also
Verweij et al., 2012). If this conclusion stands up to future research
such that the heritability of personality largely reects some combina-
tion of noisy genetic effects and reactive heritability then the argu-
ments advanced by Tooby and Cosmides (1990) a quarter century ago
would be vindicated. These very arguments have been roundly criti-
cized in the past decade as theorists characterized the adaptationist ap-
proach as being inconsistent with the existence of heritable personality
differences (e.g., Buss & Hawley, 2011; Penke, Denissen, & Miller, 2007).
It is noteworthy, therefore, that it increasingly appears they may have
been correct all along.
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ior (2015), http://dx.doi.org/10.1016/j.evolhumbehav.2015.04.001
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Rather than viewing individual differences as merely the raw material upon which selection operates, this book provides theories and empirical evidence which suggest that personality and individual differences are central to evolved psychological mechanisms and behavioral functioning. The book draws theoretical inspiration from life history theory, evolutionary genetics, molecular genetics, developmental psychology, personality psychology, and evolutionary psychology, while utilizing the theories of the "best and the brightest" international scientists working on this cutting edge paradigm shift. The first three sections analyze personality and the adaptive landscape; here, the book offers a novel conceptual framework for examining "personality assessment adaptations." Because individuals in a social environment have momentous consequences for creating and solving adaptive problems, humans have evolved "difference-detecting mechanisms" designed to make crucial social decisions such as mate selection, friend selection, kin investment, coalition formation, and hierarchy negotiation. The second section examines developmental and life-history theoretical perspectives to explore the origins and development of personality over the lifespan. The third section focuses on the relatively new field of evolutionary genetics and explores which of the major evolutionary forces-such as balancing selection, mutation, co-evolutionary arms races, and drift-are responsible for the origins of personality and individual differences.
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