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Social Epistasis Amplifies the Fitness Costs of Deleterious Mutations, Engendering Rapid Fitness Decline Among Modernized Populations

DOI:10.1007/s40806-017-0084-x
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Michael Anthony Woodley of Menie at Independent
Michael Anthony Woodley of Menie
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Matthew A. Sarraf
Matthew A. Sarraf
Matthew A. Sarraf
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Radomir N. Pestow
Radomir N. Pestow
Radomir N. Pestow
  • This person is not on ResearchGate, or hasn't claimed this research yet.
Heitor B. F. Fernandes at The University of Arizona
Heitor B. F. Fernandes
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Abstract and Figures

Deleterious mutations are typically understood exclusively in terms of their harmful effects on carrier organisms. But there are convincing reasons to think that such adverse effects are not confined to the individual level. We argue that in social species, interorganismal gene-gene interactions, which in previous literatures have been termed social epistasis, allow genomes carrying deleterious mutations to reduce via group-level pleiotropy the fitness of others, including noncarriers. This fitness reduction occurs by way of degradation of group-level processes that optimize the reproductive ecology of a population for intergroup competition through, among other mechanisms, suppression of free-riding. Such damage to group regulatory processes suggests a hidden role for the accumulation of behavior-altering "spiteful" mutations in the dynamics of the demographic transition—these mutations may have contributed to the maladaptive outcomes of this process, such as widespread subreplacement fertility. A structured population model is presented describing aspects of this social epistasis amplification model. This phenomenon is also considered as a potential explanation for the results of Calhoun’s mouse utopia experiments, which provide an opportunity to directly test a major prediction stemming from the model.
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THEORETICAL ARTICLE
Social Epistasis Amplifies the Fitness Costs of Deleterious
Mutations, Engendering Rapid Fitness Decline
Among Modernized Populations
Michael A. Woodley of Menie
1,2
&Matthew A. Sarraf
3
&Radomir N. Pestow
1
&
Heitor B. F. Fernandes
4
Published online: 21 February 2017
#Springer International Publishing 2017
Abstract Deleterious mutations are typically understood ex-
clusively in terms of their harmful effects on carrier organ-
isms. But there are convincing reasons to think that such ad-
verse effects are not confined to the individual level. We argue
that in social species, interorganismal gene-gene interactions,
which in previous literatures have been termed social epista-
sis, allow genomes carrying deleterious mutations to reduce
via group-level pleiotropy the fitness of others, including non-
carriers. This fitness reduction occurs by way of degradation
of group-level processes that optimize the reproductive ecol-
ogy of a population for intergroup competition through,
among other mechanisms, suppression of free-riding. Such
damage to group regulatory processes suggests a hidden role
for the accumulation of behavior-altering "spiteful" mutations
in the dynamics of the demographic transition—these muta-
tions may have contributed to the maladaptive outcomes of
this process, such as widespread subreplacement fertility. A
structured population model is presented describing aspects of
this social epistasis amplification model. This phenomenon is
also considered as a potential explanation for the results of
Calhoun’s mouse utopia experiments, which provide an op-
portunity to directly test a major prediction stemming from the
model.
Keywords Mutation accumulation .Mutation load paradox .
Pathological altruism .Spiteful mutations .Structured
population modeling .Social epistasis
Introduction
The Human Mutation Load Paradox
There is considerable interest in the consequences for human
populations of the relaxation of purifying selection against
deleterious, spontaneously occurring mutations (Lynch
2016). As human males age, they bequeath to their sperm
approximately two de novo base-substitution mutations per
year (Kong et al. 2012), and females bequeath around a quar-
ter of this number per year to their eggs (Wong et al. 2016).
Genomic count data indicate that offspring acquire approxi-
mately 40 to 80 de novo mutations per genome per generation
(Rahbari et al. 2016). When rarer spontaneously occurring
mutations are taken into consideration (e.g., insertion-
deletion events and copy number variation), the average off-
spring’s genome may contain as many as 100 de novo muta-
tions (Lynch 2016). It is believed that a small subset of these
mutations will be actively harmful (i.e., will produce some
pathological change in the offspring’s phenotype; Lynch
2016), and some models (Kondrashov and Crow 1993)sug-
gest that this rate of deleterious mutation theoretically requires
substantial reproductive failure (as much as 88% of individ-
uals should fail to reproduce) in order to purify a population,
coupled with significant compensatory reproduction among
the fraction participating in procreation (approximately 16
offspring per woman) in order to stave off mutational
meltdown, i.e., population collapse due to the fitness costs of
accumulating deleterious mutations.
*Michael A. Woodley of Menie
Michael.Woodley@vub.ac.be
1
Technische Universität Chemnitz, Chemnitz, Germany
2
Center Leo Apostel for Interdisciplinary Studies, Vrije Universiteit
Brussel, Brussels, Belgium
3
Cornell University, Ithaca, NY, USA
4
Department of Psychology, University of Arizona, Tucson, AZ, USA
Evolutionary Psychological Science (2017) 3:181–191
DOI 10.1007/s40806-017-0084-x
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Some of these mutations are postulated to cause psychopathology, degrade brain systems for binding moral foundations, or reduce intelligence. The rising frequency of individual pathologies is postulated to cause social pathologies, creating cultural amplifier effects as hypothesized by Dickens and Flynn (2001) and Sarraf et al. (2017). The presence of many "off-types" in the population is predicted to reduce in-group cohesion, and to favor ideological polarization and extremism that are supported by irrational beliefs. ...
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... spore productivity). A related term used previously is 'group-level pleiotropy,' used for example to refer to alleles that impact fitness of non-carriers through group-level effects (Woodley of Menie et al. 2017). 'Social pleiotropy' has also been used in the context of social animals to indicate when an individual trait impacts "several features of the social organization" (Thierry 2004) or when one locus impacts multiple social traits (Fouks et al. 2016). ...
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