Inclusive fitness theory and eusociality

TLDR: It is argued that inclusive fitness theory has been of little value in explained the natural world, and that it has led to negligible progress in explaining the evolution of eusociality, but these arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature.

Abstract: Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

Figures

Table 2 | Areas in which inclusive fitness theory has made successful predictions about behaviour in eusocial insects

Figure 2 | Co-evolution of altruism and relatedness. Evolutionary trajectories (thin curves) start with zero altruism and converge to evolutionarily stable phenotypes (black circles). Relatedness is dynamic and co-evolves with altruism. Eco-evolutionary models can predict how environmental factors (for example, habitat viscosity) affect altruism evolution. Here, viscosity decreases across trajectories from right to left, and the string of black circles shows how evolved altruism and relatedness should co-vary along an environmental gradient of habitat viscosity.

Figure 1 | Fitness landscape and Hamilton’s rule. a, Fitness landscape in resident–mutant phenotypic space. Mutant invasion (inclusive) fitness is maximized along the dashed curve and the black circle is an evolutionarily stable phenotype. However, the asymmetrical sign structure implies that evolutionary dynamics do not obey an optimizing principle12. b, Selection pressures arise from relatedness (red curve), physiological cost of altruism (blue) and change in space occupancy (black). Under weak selection, the latter is negligible (black curve close to zero) and the benefit is proportional to relatedness (see for example, equation (3) in ref. 10), which makes Hamilton’s rule a good approximation of selection10,11. The black circle indicates the evolutionarily stable phenotype found in a.

Full text

Inc lusive fitness theory and eusociality
ARISING FROM M. A. Nowak, C. E. Tarnita & E. O. Wilson Nature 466, 1057–1062 (2010)
Nowak et al.
1
argue that inclusive fitness theory has been of little value
in explaining the natural world, and that it has led to negligible pro-
gress in explaining the evolution of eusociality. However, we believe
that their arguments are based upon a misunderstanding of evolu-
tionary theory and a misrepresentation of the empirical literature. We
will focus our comments on three general issues.
First, Nowak et al.
1
are incorrect to suggest a sharp distinction
between inclusive fitness theory and ‘‘standard natural selection
theory’’. Natural selection explains the appearance of design in the
living world, and inclusive fitness theory explains what this design is
for. Specifically, natural selection leads organisms to become adapted
as if to maximize their inclusive fitness
2–4
. Inclusive fitness theory is
based upon population genetics, and is used to make falsifiable pre-
dictions about how natural selection shapes phenotypes, and so it is
not surprising that it generates identical predictions to those obtained
using other methods
2,5–7
.
Second, Nowak et al.
1
are incorrect to state that inclusive fitness
requires a number of ‘‘stringent assumptions’’ such as pairwise inter-
actions, weak selection, linearity, additivity and special population
structures. Hamilton’s original formulations did not make all these
assumptions, and generalizations have shown that none of them is
required
3,5,6,8
. Inclusive fitness is as general as the genetical theory of
natural selection itself. It simply partitions natural selection into its
direct and indirect components.
Nowak et al.
1
appear to have confused the completely general theory
of inclusive fitness with models of specific cases. Yes, researchers often
make limiting assumptions for reasons of analytical tractability when
considering specific scenarios
5,7
, as with any modelling approach. For
example, Nowak et al.
1
assume a specific form of genetic control, where
dispersal and helping are determined by the same single locus, that
mating is monogamous, and so on. However, the inclusive fitness
approach has facilitated,not hindered, empirical testingof evolutionary
theory
9–11
. Indeed, an advantage of inclusive fitness theory is that it
readily generates testable predictions in situations where the precise
genetic architecture of a phenotypic trait is unknown.
Third, we dispute the claim of Nowak et al.
1
that inclusive fitness
theory ‘‘does not provide any additional biological insight’’, delivering
only ‘‘hypothetical explanations’’, leading only to routine measure-
ments and ‘‘correlative studies’’, and that the theory has ‘‘evolved into
an abstract enterprise largely on its own’’, with a failure to consider
multiple competing hypotheses. We cannot explain these claims,
which seem to overlook the extensive empirical literature that has
accumulated over the past 40 years in the fields of behavioural and
evolutionary ecology
9–11
(Table 1). Of course, studies must consider
the direct consequences of behaviours, as well as consequences for
relatives, but no one claims otherwise, and this does not change the
fact that relatedness (and lots of other variables) has been shown to be
important in all of the above areas.
We do not have space to detail all the advances that have been made
in the areas described in Table 1. However, a challenge to the claims of
Nowak et al.
1
is demonstrated with a single example, that of sex
allocation (the ratio of investment into males versus females). We
choose sex allocation because: (1) Nowak et al.
1
argue that inclusive
fitness theory has provided only ‘‘hypothetical explanations’’ in this
field; (2) it is an easily quantified social trait, which inclusive fitness
theory predicts can be influenced by interactions between relatives;
and (3) the study of sex allocation has been central to evolutionary
work on the eusocial insects. In contrast to the claims of Nowak et al.
1
,
recent reviews of sex allocation show that the theory explains why sex
allocation varies with female density, inbreeding rate, dispersal rate,
brood size, order of oviposition, sib-mating, asymmetrical larval com-
petition, mortality rate, the presence of helpers, resource availability
and nest density in organisms such as protozoan parasites, nematodes,
insects, spiders, mites, reptiles, birds, mammals and plants
5,12,13
.
The quantitative success of this research is demonstrated by the
percentage of the variance explained in the data. Inclusive fitness
theory has explained up to 96% of the sex ratio variance in across-
species studies and 66% in within-species studies
13
. The average for all
evolutionary and ecological studies is 5.4%. As well as explaining
adaptive variation in behaviour, inclusive fitness theory has even
elucidated when and why individuals make mistakes (maladaptation),
in response to factors such as mechanistic constraints
13
. It is not
clear how Nowak et al.
1
can characterize such quantifiable success
as ‘‘meagre’’. Their conclusions are based upon a discussion in the
Supplementary Information of just three papers (by authors who
disagree with the interpretations of Nowak et al.
1
), out of an empirical
literature of thousands of research articles. This would seem to indi-
cate a failure to engage seriously with the body of work that they
recommend we abandon.
The same points can be made with regard to the evolution of the
eusocial insects, which Nowak et al.
1
suggest cannot be explained by
inclusive fitness theory. It was already known that haplodiploidy itself
may have only a relatively minor bearing on the origin of eusociality,
and so Nowak et al.
1
have added nothing new here. Inclusive fitness
theory has explained why eusociality has evolved only in monogam-
ous lineages, and why it is correlated with certain ecological condi-
tions, such as extended parental care and defence of a shared
resource
14,15
. Furthermore, inclusive fitness theory has made very
successful predictions about behaviour in eusocial insects, explaining
a wide range of phenomena (Table 2).
Ultimately, any body of biological theory must be judged on its
ability to make novel predictions and explain biological phenomena;
we believe that Nowak et al.
1
do neither. The only prediction made by
their model (that offspring are favoured to help their monogamously
Table 1
|
Inclusive fitness theory has been important in understanding a
range of behavioural phenomena
Research area Correlational? Experimental? Theory–data interplay
Sex allocation Yes Yes Yes
Policing Yes Yes Yes
Conflict resolution Yes Yes Yes
Cooperation Yes Yes Yes
Altruism Yes Yes Yes
Spite Yes Yes Yes
Kin discrimination Yes Yes Yes
Parasite virulence Yes Yes Yes
Parent–offspring conflict Yes Yes Yes
Sibling conflict Yes Yes Yes
Selfish genetic elements Yes Yes Yes
Cannibalism Yes Yes Yes
Dispersal Yes Yes Yes
Alarm calls Yes Yes Yes
Eusociality Yes Yes Yes
Genomic imprinting Yes Yes Yes
Data are taken from refs 9–11. Correlational studies test predictions using natural variation in key
variables, whereas experimental studies involve their experimental manipulation. Interplay between
theory and data means that theory has informed empirical study, and vice versa. Inclusive fitness is not
the only way to model evolution, but it has already proven to be an immensely productive and useful
approach for studying eusociality and other social behaviours.
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mated mother if this provides a sufficient benefit) merely confirms, in
a less general way, Hamilton’s original point: if the fitness benefits are
great enough, then altruism is favoured between relatives.
Patrick Abbot
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103
1
Vanderbilt University, Nashville, Tennessee 37235, USA.
2
Laboratory of Applied Entomology, Faculty of Agriculture, Shizuoka
University, Sizuoka 422-8529, Japan.
3
School of Life Sciences, PO Box 874501, Arizona State University,
Tempe, Arizona 85287-4501, USA.
4
UMR CNRS-IRD 2724, Genetics and Evolution of Infectious Diseases,
IRD, 911 Avenue Agropolis, B.P. 64501, 34394 Montpellier Cedex 5,
France.
5
Department of Zoology, University of Oxford, South Parks Road, Oxford,
OX1 3PS, UK.
e-mail: Stuart.West@zoo.ox.ac.uk
6
Department of Zoology, University of Gothenburg, SE 405 30
Gothenburg, Sweden.
7
CNRS, Universite
´
Pierre et Marie Curie, Ecole Normale Supe
´
rieure, UMR
7625, Ecologie and Evolution, 75005 Paris, France.
8
MRC Centre for Outbreak Analysis and Modelling, Department of
Infectious Disease Epidemiology, Faculty of Medicine, Imperial College, St
Mary’s Campus, Norfolk Place, London W2 1PG, UK.
9
Department of Psychology, Neuroscience and Behaviour, McMaster
University, 1280 Main St West, Hamilton, Ontario L8S 4K1, Canada.
10
IST Austria, Am Campus 1, Klosterneuburg 3400, Austria.
11
Evolutionary Genetics, Centre for Ecological and Evolutionary Studies,
Universityof Groningen, PO Box 14, NL-9750 AA Haren, The Netherlands.
12
Aarhus University, Department of Biological Sciences, Ny Munkegade
1540, 8000 Aarhus C, Denmark.
13
Department of Biology, University of Maryland, College Park, Maryland
20742-4415, USA.
14
Ecology and Evolutionary Biology, University of Colorado, Boulder,
Colorado 80309-0334, USA.
15
Faculte
´
des sciences, Rue Emile-Argand 11, Case postale 158, 2000
Neucha
ˆ
tel, Switzerland.
16
Department of Ecology and Evolutionary Biology, University of
California, 321 Steinhaus Hall, Irvine, California 92697-2525, USA.
17
Centre for Ecology and Conservation, University of Exeter, Cornwall,
Tremough, Penryn TR10 9EZ, UK.
18
Department of Ecology and Evolution, Biophore, University of
Lausanne, 1015 Lausanne, Switzerland.
19
Department of Biology, 167 Castetter Hall,MSC032020, 1 University of
New Mexico, Albuquerque, New Mexico 87131-000, USA.
20
Department of Zoology, University of Cambridge, Downing Street,
Cambridge CB2 3EJ, UK.
21
Evolution, Ecology and Genetics, Research School of Biology, Australian
National University, Canberra, ACT 0200, Australia.
22
Department of Biology and Biochemistry, University of Houston,
Houston, Texas 77204-5001, USA.
23
Institutes of Evolution, Immunology and Infection Research, School of
Biological Sciences, Ashworth Laboratories, University of Edinburgh,
Edinburgh EH9 3JT, UK.
Table 2
|
Areas in which inclusive fitness theory has made successful predictions about behaviour in eusocial insects
Trait examined Explanatory variables Correlational
studies?
Experimental
studies?
Interplay between
theory and data?
Altruistic helping Haplodiploidy versus diploidy Yes No Yes
Worker egg laying Worker policing Yes Yes Yes
Policing Relatedness Yes Yes Yes
Level of cooperation Costs, benefits and relatedness Yes Yes Yes
Intensity of work Need for work and probability of becoming queen Yes Yes Yes
Sex allocation Relatedness asymmetries due to variation in queen
survival, queen number and mating frequency
Yes Yes Yes
Sex allocation Resource availability Yes Yes Yes
Sex allocation Competition for mates betwe en related males Yes Yes Yes
Number of individuals trying to become reproductive Presence of old queens Yes Yes Yes
Workers killing queens Presence of workers, reproductives or other queens Yes No No
Exclusion of non-kin Colony membership Yes Yes Yes
Data are taken from refs 12–16.
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Department of Psychology, University of California, Santa Barbara,
Santa Barbara, California 93106-9660, USA.
25
Department of Ecology and Evolutionary Biology, Princeton University,
Princeton, New Jersey 08540, USA.
26
Department of Ecology and Evolution, The University of Chicago, 1101
E. 57 Street, Chicago, Illinois 60637, USA.
27
Department of Ecology, Montana State University, Bozeman, Montana
59717, USA.
28
Department of Biosciences, 8888 University Drive, Simon Fraser
University, Burnaby, British Columbia V5A1S6, Canada.
29
Department of Biology, Villanova University, 800 Lancaster Avenue,
Villanova, Pennsylvania 19085, USA.
30
Department of Mathematics and Statistics, Queen’s University,
Kingston, Ontario K7L 3N6, Canada.
31
The Cornell Laboratory of Ornithology, Cornell University — The
Johnson Center, 159 Sapsucker Woods Road, Ithaca, New York 14850,
USA.
32
Department of Biology, University of Louisville, Louisville, Kentucky
40292, USA.
33
Seeley G. Mudd Hall, Department of Neurobiology and Behavior,
Cornell University, Ithaca, New York 14853, USA.
34
USDA-ARS Bee Research Laboratory, BARC-E Bldg 476, Beltsville,
Maryland 20705, USA.
35
Laboratoire Ecologie and Evolution, CNRS UMR 7625, Ecole Normale
Superieure, 46 rue d’Ulm, 75005 Paris, France; Department of Ecology
and Evolutionary Biology, University of Arizona, Tucson, Ar izona 85721,
USA.
36
School of Life Sciences, John Maynard Smith Building, University of
Sussex, Brighton BN1 9QG, UK.
37
Department Biologie II Behavioral Ecology (Verhaltenso
¨
kologie),
Ludwig-Maximilians-Universita
¨
t, Mu
¨
nchen Großhaderner Str. 2
D - 82152 Planegg/Martinsried, Germany.
38
Department of Entomology, University of Kentucky, Lexington,
Kentucky 40546-0091, USA.
39
School of Life Sciences, Arizona State University, PO Box 874501,
Tempe, Arizona 85287-4501, USA.
40
CEFE - UMR 5175, 1919 route de Mende, F-34293 Montpellier Cedex
5, France.
41
School of Biological Sciences, Flinders University, GPO Box 2100,
Adelaide, South Australia 5001, Australia.
42
Kellogg Biological Station and Department of Zoology, Michigan State
University, Hickory Corners, Michigan 49060, USA.
43
School of Biology and Petit Institute for Bioengineering and Bioscience,
Georgia Institute of Technology, 310 Ferst Drive, Atlanta, Georgia
30332-0230, USA.
44
Department of Evolution and Ecology, College of Biological Sciences, 1
Shields Avenue, UC Davis, Davis, California 95616, USA.
45
Center for Pollinator Research, Huck Institutes of the Life Sciences,
Pennsylvania State University, Chemical Ecology Lab 4A, University Park,
Pennsylvania 16802, USA.
46
Muse
´
um National d’Histoire Naturelle, CP39, 12 rue Buffon, 75005
Paris, France.
47
Biology Department, University of Toronto, 3359 Mississauga Road,
Mississauga, Ont ario L5L 1C6, Canada.
48
Department of Animal and Plant Sciences, University of Sheffield,
Western Bank, Sheffield S10 2TN, UK.
49
Biologie I, Universita
¨
t Regensburg, D-93040 Regensburg, Germany.
50
Department of Biosciences, PL 65 (Viikinkaari 1), FI-00014 University
of Helsinki, Finland.
51
Department of Biology, University of Vermont, Burlington, Vermont
05405, USA.
52
School of Human Evolution and Social Change, Arizona State
University, Tempe, Arizona 85287-2402, USA.
53
Department of Animal Ecology, Institute of Ecological Science, Faculty
of Earth and Life Sciences, Vrije Universiteit, De Boelelaan 1085, NL-1081
HV Amsterdam, The Netherlands.
54
Animal Ecology Group, Centre for Evolutionary and Ecological Studies,
University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands.
55
University of Osnabrueck, Barbarastr.11, D-49076 Osnabrueck,
Germany.
56
Harvard University, Museum of Comparative Zoology, 26 Oxford St,
Cambridge, Massachusetts 02138, USA.
57
Environmental Microbiology, Swiss Federal Institute of Aquatic
Research and Technology, U
¨
berlandstrasse 133, CH-8600 Du
¨
bendorf,
Switzerland.
58
Centre for Social Evolution, Department of Biology, University of
Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.
59
School of Biological Sciences, Royal Holloway, University of London,
Egham TW20 0EX, UK.
60
Department of Ecology and Evolutionary Biology, University of
California, Santa Cruz, California 95064, USA.
61
Department of Computer Science, University of Sheffield, Sheffield
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62
Department of Anthropology and Center for Population Biology, UC
Davis, Davis, California 95616 , USA.
63
Department of Ecology and Evolutiona ry Biology, University of Arizona,
Tucson, Arizona 85721, USA.
64
Department of Zoology, 730 Van Vleet Oval, University of Oklahoma,
Norman, Oklahoma 73019, USA.
65
Department of Biology, Queen’ s University, Kingston, Ontario K7L 3N6,
Canada.
66
Integrative Biology, University of Texas at Austin, 1 University Station
C0930, Austin, Texas 78712, USA.
67
Psychologie — Universite
´
de Strasbourg, Ethologie des Primates —
DEPE (IPHC CNRS UMR 7178), 23 rue Becquerel — Strasbourg 67087,
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Department of Philosophy, University of Bristol, Bristol BS8 1TB, UK.
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Biocenter Oulu and Department of Biosciences, University of Helsinki,
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Institute of Integrative Biology, Biosciences Building, Crown Street,
University of Liverpool, Liverpool L69 7ZB, UK.
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Theoretical Biology group, University of Groningen, PO Box 14, 9750 AA
Haren, The Netherlands.
72
Department of Biology, CB#3280, Coker Hall, University of North
Carolina, Chapel Hill, NC 27599-3280, USA.
73
Department of Ecology and Evolutionary Biology, Rice University,
Houston, Texas 77005-1892, USA.
74
Department of Biochemistry, University of Zurich, Building Y27, Office
J-46, Winterthurstrasse 190, CH-8057 Zurich, Switzerland; Swiss
Institute of Bioinformatics, Quartier Sorge Ba
ˆ
timent Ge
´
nopode, CH- 1015
Lausanne, Switzerland.
75
Research Department of Genetics, Evolution and Environment, Faculty
of Life Sciences, University College London, 4 Stephenson Way, London
NW1 2HE, UK.
76
Centre for Behaviour and Evolution, Institute of Neuroscience, Faculty
of Medical Sciences, Newcastle University, Henry Wellcome Building,
Framlington Place, Newcastle upon Tyne NE2 4HH, UK.
77
School of Marine and Tropical Biology, James Cook University,
Queensland 4811, Australia.
78
Station Biologique de Roscoff, CNRS-UPMC UMR 7144, 29680
Roscoff, France.
79
Institut des Sciences de l’Evolution, University of Montpellier 2,
Montpellier 34095, France.
80
Department of Biolog y, University of North Carolina at Greensboro, 312
Eberhart Building, Greensboro, North Carolina 27403, USA.
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81
Department of Biology, 3314 Spieth Hall, University of California —
Riverside, Riverside, California 92521, USA.
82
ETH Zurich, Institute of Integrative Biology (IBZ), Universita
¨
tsstrasse 16,
CH.8092 Zu
¨
rich, Switzerland.
83
School of Philosophy, Psychology and Language Sciences, University of
Edinburgh, 3 Charles Street, Edinburgh EH8 9AD, UK.
84
School of Biology, University of St Andrews, Harold Mitchell Building, St
Andrews, Fife KY16 9TH, UK.
85
William Paterson University of New Jersey, 300 Pompton Road, Wayne,
New Jersey 07470, USA.
86
Department of Anthropology, 101 West Hall, University of Michigan,
Ann Arbor, Michigan 48109, USA.
87
Department of Entomology and Department of Animal Biology,
University of Illinois, Urbana, Illinois 61801, USA.
88
Behavioural Ecology, Institute of Ecology and Evolution, University of
Bern, Wohlenstrasse 50a, CH-3032 Hinterkappelen, Switzerland.
89
Department of Biology, University of Western Ontario, 1151 Richmond
Street North, London, Ont ario N6A 5B7, Canada.
90
Department of Anthropology, University of California, Santa Barbara,
California 93106-3210, USA.
91
Deptartment of Environmental Science, Policy and Management, 130
Mulford Hall, 3114, University of California Berkeley, Berkeley, California
94720-3114, USA.
92
Faculty of Agriculture, University of the Ryukyus, Okinawa 903-0213,
Japan.
93
Dipartimento di Biologia Evoluzionistica, Universita
`
degli Studi di
Firenze, via Romana 17, 50125 Firenze, Italy.
94
Department of Ecology and Evolutionary Biology, University of
Tennessee Knoxville, Knoxville, Tennessee 37902, USA.
95
Department of Entomology, Box 7613, North Carolina State University,
Raleigh, North Carolina 27695-7613, USA.
96
Institute for Theoretical Biology, Humboldt University zu Berlin,
Invalidenstr. 43, D-10115 Germany.
97
Departmet of Biology, Zoological Institute, K.U. Leuv en, Naamsestraat
59, B-3000 Leuven, Belgium.
98
Smithsonian Tropical Research Institute, Apartado 0843-03092,
Balboa, Panama
´
.
99
Department of Biology, 101 Morgan Building, University of Kentucky,
Lexington, Kentucky 40506-0225, USA.
100
Department of Applied Mathematics, University of Western Ontario,
1151 Richmond Street North, London, Ontario N6A 5B7, Canada.
101
Department of Human Evolutionary Biology, Harvard University,
Cambridge, Massachusetts 02138, USA.
102
Department of Biology and Program in Ecology, Evolution and
Conservation Biology, University of Nevada, Reno, Nevada 89557, USA.
103
Department of Biology, San Francisco State University, San Francisco,
California 94132, USA.
Received 20 September; accepted 17 December 2010.
1. Nowak, M. A., Tarnita, C. E. & Wilson, E. O. The evolution of eusociality. Nature 466,
1057–1062 (2010).
2. Hamilton, W. D. The genetical evolution of social behaviour, I & II. J. Theor. Biol. 7,
1–52 (1964).
3. Hamilton, W. D. Selfish and spiteful behaviour in an evolutionary model. Nature
228, 1218–1220 (1970).
4. Grafen, A. Optimisation of inclusive fitness. J. Theor. Biol. 238, 541–563 (2006).
5. Frank, S. A. Foundations of Social Evolution (Princeton Univ. Press, 1998).
6. Gardner, A., West, S. A. & Barton, N. H. The relation between multilocus population
genetics and social evolution theory. Am. Nat. 169, 207–226 (2007).
7. Rousset, F. Genetic Structure and Selection in Subdivided Populations (Princeton
Univ. Press, 2004).
8. Queller, D. C. A general model for kin selection. Evolution 46, 376–380 (1992).
9. Krebs, J. R. & Davies, N. B. Behavioural Ecology. An Evolutionary Approach 4th edn
(Blackwell Scientific, 1997).
10. Foster, K. R. A defense of sociobiology. Cold Spring Harb. Symp. Quant. Biol. 74,
403–418 (2009).
11. Westneat, D. F. & Fox, C. W. Evolutionary Behavioral Ecology (Oxford Univ. Press,
2010).
12. Hardy, I. C. W. Sex Ratios: Concepts and Research Methods (Cambridge Univ. Press,
2002).
13. West, S. A. Sex Allocation (Princeton Univ. Press, 2009).
14. Queller, D. C. & Strassmann, J. E. Kin selection and social insects. Bioscience 48,
165–175 (1998).
15. Boomsma, J. J. Lifetime monogamy and the evolution of eusociality. Phil. Trans. R.
Soc. Lond. B 364, 3191–3207 (2009).
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societies. Annu. Rev. Entomol. 51, 581–608 (2006).
Author Contributions All authors contributed to the planning, writing and/or revising
of this paper. Several others who contributed significantly are not listed because they
are named on separate comments.
Competing financial interests: declared none.
doi:10.1038/nature09831
Only full-sibling families evolved eusociality
ARISING FROM M. A. Nowak, C. E. Tarnita & E. O. Wilson Nature 466, 1057–1062 (2010)
The paper by Nowak et al.
1
has the evolution of eusociality as its title,
but it is mostly about something else. It argues against inclusive fitness
theory and offers an alternative modelling approach that is claimed to
be more fundamental and general, but which, we believe, has no prac-
tical biological meaning for the evolution of eusociality. Nowak et al.
1
overlook the robust empirical observation that eusociality has only
arisen in clades where mothers are associated with their full-sibling
offspring; that is, in families where the average relatedness of offspring
to siblings is as high as to their own offspring, independent of popu-
lation structure or ploidy. We believe that this omission makes the
paper largely irrelevant for understanding the evolution of eusociality.
Eusociality is not just any form of condition-dependent reproductive
altruism as found in cooperative breeders,but the permanentdivision of
reproductive labour. Clades where helpers became irreversibly eusocial
(ants, some bees, some wasps, and termites
2
) are old, radiated into many
subclades over evolutionary time, and achieved considerable ecological
footprints. A recent comparative study
3
showed that all hymenopteran
clades that fit the standard definition of eusociality
4
evolved from life-
time monogamous ancestors
5–8
. This implies that high relatedness
always preceded or coincided with eusociality, and contrasts with the
contention of Nowak et al.
1
that eusocialitycan evolve in any group with
parental care, or that high relatedness arises after eusociality.
Given that promiscuity is the most common mating system in
animals, strict ancestral monogamy throughout eusocial clades
implies that high relatedness was necessary for eusociality to evolve.
Nonetheless, necessity does not imply sufficiency. Monogamous
lineages may have remained solitary because the benefits of helping
at the nest were insufficient to surpass independent breeding. This is
elegantly captured by the ratio of the parameters b and c in Hamilton’s
rule. In a number of ant, bee and wasp genera the high relatedness
condition for eusociality has become secondarily relaxed via evolu-
tionary elaborations such as multiple queen mating, but this has only
occurred after worker phenotypes had specialized so that opting out to
independent breeding had become selectively disadvantageous or
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©2011

developmentally impossible
3
. Claiming (in their Supplementary Infor-
mation, Part B) that it is far simpler to consider that advanced eusocial
species just need more sperm
1
muddles proximate and ultimate expla-
nations
9,10
; many multiply-mating queens discard most of the sperm
they receive
11,12
, indicating that sperm limitation cannot explain
polyandry.
We now also know that departures from high relatedness would
almost certainly have prevented the evolution of eusociality if they had
happened before sterile castes had become permanent
8
, that is, before
reaching the point of no return to breeding independently
13
.Arecent
comparative study on birds
14
showed that cooperative breeding is an
unstable state that predominantly occurs in monogamous clades and is
likely to be lost when parents become more promiscuous. This evidence
is not merely correlative: differences in ancestral promiscuity betw een
cooperative and non-cooperative species were found even before coop-
eration arose, illustrating that monogamy preceded the evolution of
helping and that helpers leave when relatedness incentives are reduced.
This shows that high relatedness among siblings is critical along with the
Hamiltonian b/c ratio but, as in the insects, relatedness is not sufficient
because many monogamous birds are not cooperative breeders.
In light of these reconstructions of the ancestral life histories of
numerous social clades, it is surprising that the argument of Nowak
et al.
1
about eusocial evolution starts by assuming that family structure
can be replaced by any form of population structure. This assumption is
puzzling given the lack of empirical evidence that this hypothetical
‘parasocial’ route to eusociality
1,4
(where same-generation individuals
associate independent of relatedness) has produced a single extant clade
with obligately eusocial workers. We believe that this renders Part A of
the Supplementary Information of Nowak et al.
1
, and the arguments
throughout the first two-thirds of the paper, largely irrelevant to the
origin of eusociality. Part C of the Supplementary Information
addresses the evolution of sterile workers withinmonogamous or clonal
families, meaning that relatedness in these models is invariant. As a
consequence, we believe that thesemodelshave nothing to say about the
importance of relatedness in the evolution of eusociality beyond show-
ing that costs and benefits are also important. This was already clear
from Hamilton’s rule nearly half a century ago.
It should give pause for thought that none of the long-recognized
approximations of inclusive fitness theory raised in the paper was
important enough to preclude kin selection theory from developing
into a well-integrated network of complementary hypotheses with
high predictive power for reproductive decision-making in real-world
social organisms. In contrast, the abstractions of Nowak et al.
1
fail to
provide any new predictions or questions; all they apparently have to
offer is the truism that helpers are associated with longer-lived, fecund
breeders.
Jacobus J. Boomsma
1
, Madeleine Beekman
2
, Charlie K. Cornwallis
3
,
Ashleigh S. Griffin
3
,LukeHolman
1
, William O. H. Hughes
4
,
Laurent Keller
5
,BenjaminP.Oldroyd
2
& Francis L. W. Ratnieks
6
1
Centre for Social Evolution, Department of Biology, University of
Copenhagen, 2100 Copenhagen, Denmark.
e-mail: JJBoomsma@bio.ku.dk
2
Behaviour and Genetics of Social Insects Lab, School of Biological
Sciences A12, University of Sydney, New South Wales, Australia.
3
Department of Zoology, University of Oxford, South Parks Road, Oxford
OX1 3PS, UK.
4
Institute of Integrative and Comparative Biology, Miall Building,
University of Leeds, Leeds LS2 9JT, UK.
5
Department of Ecology and Evolution, Biophore, University of Lausanne,
1015 Lausanne, Switzerland.
6
Laboratory of Apiculture and Social Insects, School of Life Sciences,
University of Sussex, Falmer, Brighton BN1 9QG, UK.
Received 19 September; accepted 17 December 2010.
1. Nowak, M. A., Tarnita, C. E. & Wilson, E. O. The evolution of eusociality. Nature 466,
1057–1062 (2010).
2. Inward, D. J. G., Vogler, A. P. & Eggleton, P. A comprehensive phylogenetic analysis
of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol.
Phylogenet. Evol. 44, 953–967 (2007).
3. Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. Ancestral
monogamy shows kin selection is key to the evolution of eusociality. Science 320,
1213–1216 (2008).
4. Wilson, E. O. The Insect Societies (Belknap Press of Harvard Univ. Press, 1971).
5. Hamilton, W. D. The genetical evolution of social behaviour, I & II. J. Theor. Biol. 7,
1–52 (1964).
6. Alexander, R. D. The evolution of social behavior. Annu. Rev. Ecol. Syst. 5, 325–383
(1974).
7. Charnov, E. L. Evolution of eusocial behavior: offspring choice or parental
parasitism? J. Theor. Biol. 75, 451–465 (1978).
8. Boomsma, J. J. Kin selection versus sexual selection: Why the ends do not meet.
Curr. Biol. 17, R673–R683 (2007).
9. Mayr, E. Cause and effect in biology. Science 134, 1501–1506 (1961).
10. Tinbergen, N. On aims and methods of ethology. Z. Tierpsychol. 20, 410–433
(1963).
11. Baer, B. Sexual selection in Apis bees. Apidologie (Celle) 36, 187–200 (2005).
12. den Boer, S. P. A. et al. Prudent sperm use by leaf-cutter ant queens. Proc. R. Soc.
Lond. B 276, 3945–3953 (2009).
13. Wilson, E. O. One giant leap: How insects achieved altruism and colonial life.
Bioscience 58, 17–25 (2008).
14. Cornwallis, C. K., West, S. A., Davis, K. E. & Griffin, A. S. Promiscuity and the
evolutionary transition to complex societies. Nature 466, 969–972 (2010).
Author Contributions J.J.B. took the initiative for this contribution and wrote the first
draft. All co-authors provided written and/or oral comments that helped shape the
final submission.
Competing financial interests: declared none.
doi:10.1038/nature09832
Kin selection and eusociality
ARISING FROM M. A. Nowak, C. E. Tarnita & E. O. Wilson Nature 466, 1057–1062 (2010)
Hamilton
1
described a selective process in which individuals affect kin
(kin selection), developed a novel modelling strategy for it (inclusive
fitness), and derived a rule to describe it (Hamilton’s rule). Nowak
et al.
2
assert that inclusive fitness is not the best modelling strategy,
and also that its production has been ‘‘meagre’’. The former may be
debated by theoreticians, but the latter is simply incorrect. There is
abundant evidence to demonstrate that inclusive fitness, kin selection
and Hamilton’s rule have been extraordinarily productive for under-
standing the evolution of sociality.
Below we list a few examples of what has been learned from applying
kin selection theory—there are thousands of others. (1) Organisms
overwhelmingly direct costly assistance, and all true altruism, towards
kin
3
. (2) Eusociality in insects originated in organisms with parental
care and single mating, which means that relatedness among helpers
and brood is generally at the level of siblings
4
. (3) Benefits that can
make helping more profitable than reproducing independently often
take the forms of either fortress defence (termites, naked mole rats,
social shrimp, social thrips and aphids, and some ants) or life insurance
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24 MARCH 2011 | VOL 471 | NATURE | E5
Macmillan Publishers Limited. All rights reserved
©2011

Frequently asked questions

Q1. What are the contributions mentioned in the paper "Inclusive fitness theory and eusociality" ?

However, the authors believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. Third, the authors dispute the claim of Nowak et al. that inclusive fitness theory ‘ ‘ does not provide any additional biological insight ’ ’, delivering only ‘ ‘ hypothetical explanations ’ ’, leading only to routine measurements and ‘ ‘ correlative studies ’ ’, and that the theory has ‘ ‘ evolved into an abstract enterprise largely on its own ’ ’, with a failure to consider multiple competing hypotheses. The authors can not explain these claims, which seem to overlook the extensive empirical literature that has accumulated over the past 40 years in the fields of behavioural and evolutionary ecology ( Table 1 ). Of course, studies must consider the direct consequences of behaviours, as well as consequences for relatives, but no one claims otherwise, and this does not change the fact that relatedness ( and lots of other variables ) has been shown to be important in all of the above areas. The authors do not have space to detail all the advances that have been made in the areas described in Table 1. However, a challenge to the claims of Nowak et al. is demonstrated with a single example, that of sex allocation ( the ratio of investment into males versus females ). The authors choose sex allocation because: ( 1 ) Nowak et al. argue that inclusive fitness theory has provided only ‘ ‘ hypothetical explanations ’ ’ in this field ; ( 2 ) it is an easily quantified social trait, which inclusive fitness theory predicts can be influenced by interactions between relatives ; and ( 3 ) the study of sex allocation has been central to evolutionary work on the eusocial insects. In contrast to the claims of Nowak et al., recent reviews of sex allocation show that the theory explains why sex allocation varies with female density, inbreeding rate, dispersal rate, brood size, order of oviposition, sib-mating, asymmetrical larval competition, mortality rate, the presence of helpers, resource availability and nest density in organisms such as protozoan parasites, nematodes, insects, spiders, mites, reptiles, birds, mammals and plants. The quantitative success of this research is demonstrated by the percentage of the variance explained in the data. Their conclusions are based upon a discussion in the Supplementary Information of just three papers ( by authors who disagree with the interpretations of Nowak et al. ), out of an empirical literature of thousands of research articles. This would seem to indicate a failure to engage seriously with the body of work that they recommend the authors abandon. First, Nowak et al. are incorrect to suggest a sharp distinction between inclusive fitness theory and ‘ ‘ standard natural selection theory ’ ’. The same points can be made with regard to the evolution of the eusocial insects, which Nowak et al. suggest can not be explained by inclusive fitness theory. Furthermore, inclusive fitness theory has made very successful predictions about behaviour in eusocial insects, explaining a wide range of phenomena ( Table 2 ). Ultimately, any body of biological theory must be judged on its ability to make novel predictions and explain biological phenomena ; the authors believe that Nowak et al. do neither. 

Q2. What is the way to explain the evolution of sociality?

There is abundant evidence to demonstrate that inclusive fitness, kin selection and Hamilton’s rule have been extraordinarily productive for understanding the evolution of sociality. 

Q3. What is the way to test the idea of eusociality?

monogamy and sex ratio manipulation may be important for the evolution of eusociality; such ideas are best tested in the context of the explicit model that the authors propose. 

Q4. What is the key to the evolution of eusociality?

4. Hughes, W., Oldroyd, B., Beekman, M. & Ratnieks, F. Ancestral monogamy shows kin selection is key to the evolution of eusociality. 

Q5. What are the other clades where helpers became irreversibly eusocial?

Clades where helpers became irreversibly eusocial (ants, some bees, some wasps, and termites2) are old, radiated into many subclades over evolutionary time, and achieved considerable ecological footprints. 

Q6. What is the meaning of the phrase ‘defence and care of young with mass provisioning?

Bees are mass provisioners, as Herre and Wcislo6 say, and the authors should have used the phrase ‘defence and care of young with mass provisioning (bees) or progressive provisioning (others)’. 

Q7. What did the authors find out about the evolution of eusociality?

A recent comparative study3 showed that all hymenopteranclades that fit the standard definition of eusociality4 evolved from lifetime monogamous ancestors5–8. 

Q8. What are the coefficients of relationship for a neighbour?

The fractions in question are simply the coefficients of relationship appropriate to the neighbours whom he affects: unity for clonal individuals, one-half for sibs, one-quarter for half-sibs, one-eighth for cousins,...and finally zero for all neighbours whose relationship can be considered negligibly small. 

Q9. What does the author think of the proposed alternative?

if the non-eusocial, haplodiploid species pose a problem for inclusive fitness, then the fact that hundreds of them also make nests (including many living in communal or subsocial groups) does not support the proposed alternative.