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Inclusive fitness: 50 years on

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Abstract

The cardinal problem of evolutionary biology is to explain adaptation, or the appearance of design in the living world [[1][1],[2][2]]. Darwin [[3][3]] convincingly argued that the process of adaptation is driven by natural selection: those heritable variations—i.e. genes—that are associated
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Introduction
Cite this article: Gardner A, West SA. 2014
Inclusive fitness: 50 years on. Phil.
Trans. R. Soc. B 369: 20130356.
http://dx.doi.org/10.1098/rstb.2013.0356
One contribution of 14 to a Theme Issue
‘Inclusive fitness: 50 years on’.
Subject Areas:
behaviour, evolution, genetics, ecology,
theoretical biology, health and disease
and epidemiology
Keywords:
social evolution, adaptation, altruism,
kin selection, natural selection, theory
Author for correspondence:
Andy Gardner
e-mail: andy.gardner@st-andrews.ac.uk
Inclusive fitness: 50 years on
Andy Gardner
1
and Stuart A. West
2
1
School of Biology, University of St Andrews, Dyers Brae, St Andrews KY16 9TH, UK
2
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
1. Introduction
The cardinal problem of evolutionary biology is to explain adaptation, or the
appearance of design in the living world [1,2]. Darwin [3] convincingly
argued that the process of adaptation is driven by natural selection: those heri-
table variations—i.e. genes—that are associated with greater individual
reproductive success are those that will tend to accumulate in natural popu-
lations. To the extent that the individual’s genes are causally responsible for
her improved fitness, natural selection leads to the individual appearing
designed as if to maximize her fitness. Thus, Darwinism is a theory of both
the process and the purpose of adaptation.
However, correlations between an individual’s genes and her fitness need
not reflect a direct, causal relationship. For example, genes for altruism can
be associated with greater fitness, despite the direct cost that they inflict on
their bearer, if relatives interact as social partners. This is because an individual
who carries genes for altruism will tend to have more altruistic social partners.
That altruism can be favoured by natural selection suggests that the purpose of
adaptation is not, in general, to maximize the individual’s personal fitness [4].
Although Darwin [3] recognized the potential for such indirect effects to
drive the evolution of social behaviours, discussing the logic of kin selection
theory in connection with the adaptations of sterile insect workers, it was
William D. Hamilton (figure 1), more than a century later, who developed
these insights into a full mathematical theory. By quantifying the relative
strengths of direct selection, acting via the individual’s own reproduction,
and indirect selection, acting via the reproduction of the individual’s relatives,
Hamilton [4] revealed the ultimate criterion that natural selection uses to judge
the fate of genes.
Hamilton’s rule states that any trait—altruistic or otherwise—will be
favoured by natural selection if and only if the sum of its direct and indirect fit-
ness effects exceeds zero [47]. That is c þ
P
i
b
i
r
i
. 0, where c is the impact
that the trait has on the individual’s own reproductive success, b
i
is its impact
on the reproductive success of the individual’s ith social partner and r
i
is the
genetic relatedness of the two individuals. This mathematical partition of fit-
ness effects underpins the kin selection approach to evolutionary biology [8].
The general principle is that with regards to social behaviours, natural selection
is mediated by any positive or negative consequences for recipients, according
to their genetic relatedness to the actor. Consequently, individuals should show
greater selfish restraint, and can even behave altruistically, when interacting
with closer relatives [4].
Ha ving clarified the process of social adapta t ion, Hamilton [4] revealed its true
purpose: to maximize inclusive fitness (figure 2). That is, Darwinian individuals
should strive to maximize the sum of the fitness effects that the y hav e on all
their r ela tiv es (including themselves), each increment or decrement being weighte d
by their genetic relatedness. This is the most fundamental revision that has been
made to the logic of Darwinism and—aside fr om a possibly apocryphal quip
attributed to J. B. S. Haldane, to the effect that he would giv e his life to sav e the
lives of two brothers or eight cousin s—it was wholly original to Hamilton.
Since its inception 50 years ago, inclusive fitness theory has grown to
become one of the most successful approaches in evolutionary biology. In
addition to igniting an explosive interest in altruistic behaviour, it also ener-
gized the investigation of many other social traits (table 1). In all its
&
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applications, the usefulness of inclusive fitness theory, and
its encapsulation in Hamilton’s rule, lies in how it provides
a simple conceptual framework that can be applied with rela-
tive ease to a wide range of scenarios, successfully translating
between the dynamical process of natural selection and the
design objective of Darwinian adaptation, on paper, in the
laboratory and in the field [911].
In addition to its traditional focus upon individual
organisms, inclusive fitness theory has been applied equally
successfully to explain social interactions between genes,
illuminating the evolution of selfish genetic elements
and genomic imprinting [12,13]. Indeed, by translating
between—and characterizing conflicts of interest within—
different levels of biological organization, inclusive fitness
theory provides a framework for understanding major
transitions in individuality (table 2; [14]).
Clearly, inclusive fitness is not a single hypothesis, but
rather represents an entire programme of research. Scientific
hypotheses are judged according to how amenable they are
for empirical testing and how well they resist attempts at
empirical falsification. By contrast, scientific research pro-
grammes are judged according to how well they facilitate
the formulation and testing of hypotheses—that is, stimulat-
ing the interplay between theory and empiricism that drives
progress in scientific understanding. For example, inclusive
fitness theory has yielded a number of hypotheses concerning
the factors driving the evolution of insect eusociality, includ-
ing the ‘haplodiploidy hypothesis’ [4,18] and the ‘monogamy
hypothesis’ [ 1921]. The former hypothesis has not with-
stood detailed theoretical and empirical scrutiny, whereas
the latter goes from strength to strength [1925]. This is
exactly what we expect of a productive research programme.
In order to better assess the health of inclusive fitness
theory on its 50th anniversary, here we showcase research
showing the research programme in action, from the ext-
remely pure, mathematical realm, through basic empirical
science, to bold applications in a variety of disciplines.
The first three papers of this theme issue explore the
connections between inclusive fitness and the classical foun-
dations of evolutionary theory, with Laurent Lehmann and
Franc¸ois Rousset focusing upon population genetics, Allen
Moore and co-workers focusing upon quantitative genetics,
and David Queller revisiting the central mathematical result
of Darwinian theory—Fisher’s fundamental theorem of natu-
ral selection—from a social evolutionary perspective. These
contributions are followed by an exploration of alternative
mathematical approaches to inclusive fitness, with Peter
Taylor and Wes Maciejewski considering social evolution in
structured populations from a graph-theoretic angle and
Hisashi Ohtsuki developing connections with game theory.
Moving on to specific biological questions, Geoff Wild
and Cody Koykka explore the evolution of cooperative breed-
ing from a theoretical perspective, whereas Andrew Bourke
and Ben Hatchwell and co-workers take the stock of the
empirical successes of inclusive fitness theory on this front,
illustrating comparative and focused field approaches,
respectively. Descending to the level of the gene, Ben Nor-
mark and Laura Ross investigate the role for inclusive
fitness conflicts to drive the evolution of genetic systems.
This basic research is then followed by more applied uses
of inclusive fitness theory. Helen Leggett and co-workers
explore the insights that inclusive fitness theory yields for
infectious disease, and Bernard Crespi and co-workers
broaden out this exploration to consider non-infectious dis-
ease and ‘Hamiltonian medicine’, in general. We close the
theme issue with Toby Kiers and Ford Denison’s exploration
of applications of inclusive fitness theory to agriculture,
and Thom Scott-Phillips and co-workers on its application
to understanding human culture.
These contributions confirm that inclusive fitness theory
is in excellent shape. It still dominates the study of social
interactions in behavioural ecology, and continues to break
new ground in other disciplines. This is a testament not
only to the generality and flexibility of the theory, but also
to the efforts of its practitioners, including both theoreti-
cians who maintain a firm grasp on the natural world and
empiricists who keep a close eye on the latest theoretical
developments. Hamilton was one of those rare individuals
Figure 1. William D. Hamilton (19362000). Copyright: Tokyo Zoological
Park Society.
b
c
Figure 2. Inclusive fitness comprises the effects that the actor has on her
own reproductive success and the reproductive success of her relatives
(solid arrows), but not the effects that her relatives have on her reproductive
success or on their own reproductive success (dashed arrows). If an action
incurs a direct fitness cost of c to the actor’s own fitness, and provides an
indirect fitness benefit of b to her social partner, then natural selection
favours that action if rb 2 c . 0, where r is the genetic relatedness of
the two individuals [4].
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who effortlessly combined theory with forays into the field,
but most of the rest of us who specialize one way or the
other need to communicate and collaborate to achieve
the requisite interplay of theory and empiricism. Science is
a social enterprise, so it may be unsurprising that inclusive
fitness theory epitomizes the successful scientific research
programme. The next 50 years promise to be very exciting.
References
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Table 2. The major transitions in individuality, according to Bourke [14].
major transition in
individuality details
prokaryotic cell separate replicators (genes) ! cell
enclosing genome
eukaryotic cell separate unicells ! symbiotic unicell
sexual reproduction asexual unicells ! sexual unicell
multicellularity unicells ! multicellular organism
eusociality multicellular organisms ! eusocial
society
interspecific mutualism separate species ! interspecific
mutualism
Table 1. Some example areas where inclusive fitness theory has facilitated
insights and understanding. Inclusive fitness theory is not the only way to
model evolution, but it has proved to be an immensely productive and
useful approach for studying social behaviours [917].
research areas
adoption, alarm calls, altruism, cannibalism, conflict resolution,
cooperation, dispersal, division of labour, eusociality, kin
discrimination, genomic imprinting, multicellularity, mutualism,
parasite virulence, parentoffspring conflict, policing, selfish genetic
elements, sex allocation, sibling conflict, spite, suicide and
symbiosis.
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... Although the theory of inclusive fitness offers a possible interpretation of how the germ/soma separation can evolve, we think that this interpretation is more complex than this theory suggests, as many more mechanisms, not necessarily altruistic, may underlie its evolution (Okasha 2006;Nowak et al. 2010;Durand 2020). This is because the concept of biological altruism has a very specific meaning (Gardner and West 2014), and not every biological mechanism underlying the evolution of the germ/soma separation is of this type. To say that a given behavior is altruistic, it must be performed by the organism as a means of reducing its direct fitness and substantially enhancing its indirect fitness. ...
... Rather, we wish to show that the observation of some costly behaviors that diminish the reproductive capabilities of their bearers, while simultaneously leading to an increase in the number of these very genes in the population, does not necessarily mean that this behavior is caused by altruism driven by kin selection. For this behavior to be caused by altruism, the actor must have been in control of it (Gardner and West 2014). Our article shows that, in many situations, somatic cells are not in control; on the contrary, they are coerced to behave in this costly way, and thus even if an increase in their number of genes in the population follows, this is only accidental. ...
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