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Insights and opportunities in insect social behaviorRaghavendra Gadagkar, Deborah Gordon, Laurent Keller,
Rick Michod, David Queller, Gene E Robinson,
Joan Strassmann and Mary Jane West-Eberhard
Current Opinion in Insect Science 2019, 34:ix–xx
For a complete overview see the Issue
https://doi.org/10.1016/j.cois.2019.08.009
2214-5745/ã 2019 Published by Elsevier Inc.
We asked several scientists who (among many others) have made key
contributions to the study of social behavior in insects to share their thoughts
about two broad questions. The first is: With respect to where we are in our
understanding of the evolution of social behavior, are there a couple of key
insights you had over the course of your career that you would be willing to
share? And the second is: What kinds of questions or opportunities would
you hope that young scientists will embrace in coming years in the study of
sociality and major transitions, and/or what is missing in the field? Their
answers, which we encouraged ‘off the cuff’ and by email, are compiled
below. We have lightly edited their answers in spots, adding a comma here or
inserting a word there, and any mistakes in that regard are entirely our own.
Sarah Kocher and Patrick Abbot
Dr Gadagkar is a professor at the Centre for Ecological Sciences at the
Indian Institute of Science. His research combines work in the field and
laboratory to develop and test theoretical predictions about the evolution of
social behavior, and the relative roles of genetic relatedness, ecology,
physiology and demography in social evolution, deriving insights from
the species he has long studied, the primitively eusocial tropical wasp,
Ropalidia marginata.
With respect to where we are in our understanding of the evolution of social
behavior, are there a couple of key insights you had over the course of your
career that you would be willing to share?
I am not sure I want to call them ‘key insights’ but the following are three
concerns I have long had about out our endeavour to provide an evolutionary
explanation of social behaviour.
Our attempts to understand the evolution of social behaviour have largely
been overshadowed by one goal, namely, to solve the apparent paradox of
Raghavendra Gadagkar
Centre for Ecological Sciences, IndianInstitute of Science, India
Deborah Gordon
Department of Biology, Stanford University,United States
Laurent Keller
Department of Ecology and Evolution,University of Lausanne, Switzerland
Rick Michod
Department of Ecology and Evolution,University of Arizona, United States
David Queller
Department of Biology, WashingtonUniversity in St. Louis, United States
Gene E Robinson
Carl R. Woese Institute for Genomic Biology,Department of Entomology, andNeuroscience Program, University of Illinoisat Urbana-Champaign, United States
Joan Strassmann
Department of Biology, WashingtonUniversity in St. Louis, United States
Mary Jane West-Eberhard
Smithsonian Tropical Research Institute, c/oEscuela de Biologia, Universidad de CostaRica, Costa Rica
Available online at www.sciencedirect.com
ScienceDirect
www.sciencedirect.com Current Opinion in Insect Science 2019, 34:ix–xx
x Social insects
altruism. How can natural selection promote self-sacrific-
ing behaviour? Other questions such as the evolution of,
division of labour, kin and nestmate recognition, cooper-
ative brood care, nest building, foraging and prey capture,
communication, polyandry, serial or simultaneous polyg-
yny, dispersal and colony founding and so on, have
received marginal attention, due to a perception of not
being sexy enough or of being logical downstream con-
sequences of the evolution of altruistic group living. This
is unfortunate and needs course correction so that the
other phenomena listed above have a rightful place of
their own and we are open to the reverse possibility of
altruism itself being the downstream consequence of the
evolution of these phenomena.
The prevailing solutions to the paradox of altruism have
been framed in varying ways that themselves have evolved
over time. In the 1970’s and 80’s kin selection, mutualism
and parental manipulation were the dominant paradigms,
sometimes seen as competing explanations and sometimes
as complementary [1–3]. Without any satisfactory conclu-
sions regarding the relative roles of these forces, the 1990’s
and early 2000’s saw the rise of kin selection at the cost of
the other two, but framed largely in terms of inclusive
fitnessandHamilton’s rule [e.g.Gadagkar [4]]. Even before
Hamilton’s rule was tested with simultaneous and ade-
quate attention to all three parameters namely cost, benefit
and relatedness, we are now in the midst of a bitter and
unproductive controversy about the very validity of inclu-
sive fitness and utility of Hamilton’s rule [5,6]. Without
even a preliminary resolution of the issues raised by this
controversy, focus is being shifted to group selection and
multilevel selection [7]. There have been fascinating new
discoveries regarding proximate factors implicated in the
evolution of social behaviour such as altruistic genes,
developmental pathways and epigenetics (see below),
but their relevance to the original evolutionary questions
remain largely unarticulated. Attempts at producing a
metatheory have barely taken off [8]. Without discarding
any theory, the attention we pay to different theories has
waxed and waned according to prevailing fashions. Is this
adequate progress?
What exactly do we demand from a theory of social
evolution? Any theory should make testable predictions
but is it adequate that the theory makes some testable
predictions regrading some of the phenomena? What
about the many phenomena that remain unaddressed
by the theory? Is the function of empirical research
merely to test predictions of the theory or is the function
of the theory to explain the various phenomena discov-
ered by empirical research? How general or specific
should the theory be? Should its predictions apply to
all taxonomic groups with social behaviour? Is it OK to
have different theories for different taxonomic groups and
different subphenomena of social behaviour? Should the
theory predict the distribution of social behaviour and its
Current Opinion in Insect Science 2019, 34:ix–xx
variation across taxonomic groups or only be applied after
social behaviour has been discovered and described [9]? Is
it adequate that a theory is sufficient to explain some
phenomenon without actually being necessary, because
other theories can also do the same [10]?
What kinds of questions or opportunities would you hope
that young scientists will embrace in coming years in the
study of sociality and major transitions, and/or what is
missing in the field?
The landscape of social insect research has changed
rather dramatically during the last 40 years that I have
been personally involved. Natural history, taxonomy,
biogeography, ecology, behaviour and speculation about
the evolutionary transitions from solitary, to primitively
eusocial, to highly eusocial, were the major themes of
nearly all research in approximately the first half of this
period (the last two decades of the 20th century). In the
first two decades of the 21st century, nearly all of these
themes have become old-fashioned, and are addressed
only by a shrinking minority of the social insect research
community. Understanding the genetic, molecular and
developmental mechanisms of a small number of already
known phenomena in an even smaller number of model
species is today the dominant, sexy, state-of-the-art,
prestigious, modern, respectable theme of research. This
new kind of research has been made possible by the
spectacular advances in technology in the fields of molec-
ular biology, genetics and developmental biology and by
great advances in our understanding of these phenomena
in other model organisms such as Drosophila. This has
revolutionized the study of social insects and taken our
understanding of social behaviour and social evolution to
a significant new level. Today we are beginning to under-
stand the molecular basis of the honey bee dance lan-
guage, altruistic behaviour, division of labour, and caste
differentiation, to take just a few examples [11–14].
These developments are very welcome and encouraging.
Indeed, it would have been unfortunate if social insects
researchers had failed to take advantage of the new
technology sweeping the life sciences. And yet, these
developments appear to have come with a significant cost.
The social insect community is focusing rather exces-
sively on understanding the molecular mechanisms of
already known phenomena. Spectacular progress in social
insect research of the kind we have seen in recent times is
only sustainable if we continue to invest resources and
people in ‘old-fashioned’ natural history, ecology and
behaviour. Most social insect species remain undescribed,
many tropical habitats expected to contain rich biodiver-
sity remain unexplored and we can safely expect that
many facets of social life remain to be discovered. We
must restore social prestige in natural history, reward
intrepid naturalists travelling deep into tropical forests
and discovering new species and new phenomena and
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Insights and opportunities in insect social behavior Gadagkar et al. xi
take care not to relegate phenomena not yet studied at the
molecular level to second class science. Ideally, natural
history and related disciplines should constitute the large
base and the molecular biology of social behaviour should
be the small tip of the research pyramid [15].
Studying the molecular mechanisms that make social
behaviour possible requires access to well-equipped lab-
oratories and significant infrastructure and funding. It is
best done by a minority of the research community that
can command such resources. The vast majority of
researchers who cannot command the required resources
should not be forced to do molecular biology at a subop-
timal level but must be encouraged and empowered to do
first-rate natural history. Researchers from economically
backward but biodiversity rich countries in Asia, Africa
and Latin America are ideally placed to do first-rate
natural history and discover new species and new phe-
nomena and feed the molecular biologists with new
research questions [16]. It is sadly ironical that these
researchers are often under pressure to use the meagre
resources of their countries to enter into a losing compe-
tition with laboratories in advanced countries to study the
molecular biology of social behaviour, instead of proudly
studying the rich biodiversity in their backyard, at a
fraction of the cost. The onus is on research policy makers
in the developing countries to create an environment
where their scientists can undertake with pride, the kind
of research that they can do best.
References
1. Alexander, RD: The evolution of social behavior. Annu.Rev. Ecol. Syst. 1974, 5:325-383.
2. Hamilton, WD: Altruism and related phenomena,mainly in Social Insects. Annu. Rev. Ecol. Syst. 1972,
3:192-232.
3. Lin, N and Michener, CD: Evolution of sociality ininsects. Q. Rev. Biol. 1972, 47:131-159.
4. Gadagkar R: The social biology of Ropalidia marginata:
Toward understanding the evolution of eusociality. Har-
vard University Press; 2001.
5. Nowak, MA, Tarnita, CE, and Wilson, EO: Theevolution of eusociality. Nature 2010, 466:1057-1062.
6. Abbot, P, Abe, J, Alcock, J, Alizon, S, Alpedrinha, JAC,
Andersson, M, Andre, J-B, van Baalen, M, Balloux, F,
Balshine, S et al.: Inclusive fitness theory and eusociality.Nature 2011, 471:E1-E4.
7. Wilson, DS and Wilson, EO: Rethinking the theoreticalfoundation of sociobiology. Quart. Rev. Biol. 2007, 82:327-348.
www.sciencedirect.com
8. Lehmann, L and Keller, L: The evolution of coopera-tion and altruism - a general framework and a classifica-tion of models. J. evol. Biol. 2006, 19:1365-1376.
9. Gadagkar, R: Social Evolution: Does Collapsing Tax-onomic Boundaries Produce a Synthetic Theory? AReview of - Comparative Social Evolution, (Eds.) D. R.Rubenstein and P. Abbot, Cambridge University Press,Cambridge, New York (2017). Quart. Rev. Biol. 2018,
93:121-125.
10. Gadagkar, R: Evolution of social behaviour in theprimitively eusocial wasp Ropalidia marginata: do we needto look beyond kin selection? Phil. Trans. R. Soc. B 2016,
371:1-8.
11. Barron, AB, Maleszka, R, Vander Meer, RK, and
Robinson, GE: Octopamine modulates honey bee dancebehavior. Proc. Natl. Acad. Sci. USA 2007, 104:1703-1707.
12. Chandra, V, Fetter-Pruneda, I, Oxley, PR, Ritger, AL,
McKenzie, SK, Libbrecht, R, and Kronauer, DJC: Socialregulation of insulin signaling and the evolution of euso-ciality in ants. Science 2018, 361:398-402.
13. Lattorff, HMG and Moritz, RFA: Genetic underpin-nings of division of labor in the honeybee (Apis mellifera).Trends in Genetics 2013, 29:641-648.
14. Thompson, GJ, Hurd, PL, and Crespi, BJ: Genesunderlying altruism. Biol Lett 2013, 9:0395.
15. Gadagkar, R: The birth of ant genomics. Proc. Natl.Acad. Sci. USA 2011, 108:5477-5478.
16. Gadagkar, R: Science as a hobby: how and why I cameto study the social life of an Indian primitively eusocialwasp. Current Science 2011, 100:845-858.
Dr Gordon is a professor in the Department of Biology at
Stanford University. She studies how collective behaviors
emerge without central control. She has developed long-
term field studies on the harvester ant, Pogonomyrmexbarbatus to examine how individual behavioral variation
can organize colony-level behavior.
With respect to where we are in our understanding of the
evolution of social behavior, are there a couple of key
insights you had over the course of your career that you
would be willing to share?
Current Opinion in Insect Science 2019, 34:ix–xx
xii Social insects
I started out thinking about how to understand colony
behavior as the aggregate of the actions of individuals, and
found that ants use the rate or pattern of simple olfactory
interactions to decide what to do. I learned that the best
way to find out how social behavior is organized is to think
about how it changes in response to changing conditions.
Learning about the diverse behavior of different ant
species in different habitats has led to an ecological
perspective on the evolution of social behavior. It seems
to me that the key to learning about the evolution of social
behavior is to focus on the correspondence between how
the environment changes and the dynamics of the feed-
back created by social interactions.
There are 14 000 species of ants that operate in every
conceivable habitat. I know a few of them: harvester ants
in New Mexico, the invasive Argentine ant and the native
winter ant in northern California, the arboreal turtle ant in the
tropical dry forest in Mexico, and, in shorter engagements,
Lasius fuliginosus in England, red wood ants in Finland, and
the red imported fire ant transported into the lab.
Comparing the collective behavior of different ant species
suggests a general framework for the relation between the
dynamics of collective behavior and its environment. One
important feature of the environment is stability, the
frequency of change in the conditions associated with
the behavior, and the threat of rupture. Another is the
relation the environment poses between intake and costs
- how much the behavior brings in and how much is used
to accomplish it. Another is the distribution of resources
in space and time, such as scattered or patchy.
Social behavior differs according to the dynamics of each
species’ environment. Species differ in how feedback
from social interactions regulates the rate at which activi-
ties are initiated, stopped, and how quickly they amplify.
For example, ant species that use rapidly changing,
patchy resources use trail pheromone to create a form
of positive feedback that rapidly amplifies the number of
ants on the trail, while species that forage for scattered,
stable resources do not make trails. Amplification is
related to a second feature: how the feedback generated
by interactions makes it easy or difficult to instigate the
behavior. If positive feedback is required, then the
default is not to start until the positive feedback occurs.
By contrast, when feedback is negative, the default is to
keep going unless something negative occurs. For exam-
ple, harvester ants in the desert, where water is limited, do
not go out to forage, an activity that entails water loss,
unless they meet enough successful foragers coming in for
food. Natural selection is shaping how colonies regulate
foraging activity in response to water stress. By contrast,
turtle ants in the tropical canopy, foraging in a humid
environment, keep going unless they meet a competing
species.
Current Opinion in Insect Science 2019, 34:ix–xx
To learn about the evolution of social behavior, rather
than attempting to count up the benefits of each indivi-
dual’s actions independently, we can ask how selection on
individual behavior depends on how the network of
relations it is in responds to changing conditions.
Gordon DM 2010. Ant Encounters: Interaction Networks
and Colony Behavior. Princeton: Princeton Univ Press.
2013. Gordon, D.M. The rewards of restraint in the
collective regulation of foraging by harvester ant colonies.
Nature. DOI: 10.1038/nature12137
2016. Gordon, D. M. The evolution of the algorithms for
collective behavior. Cell Systems 3:514-520 DOI:
10.1016/j.cels.2016.10.013
2017. Gordon, D. M. Local regulation of trail networks of
the arboreal turtle ant, Cephalotes goniodontus. American
Naturalist. DOI: 10.1086/693418
2018. Pagliara R., Gordon DM, Leonard NE. Regulation
of harvester ant foraging as a closed-loop excitable sys-
tem. PLoS Computational Biology DOI: 10.1371/journal.
pcbi.1006200
2019. Gordon, D. M. The ecology of collective behavior
in ants. Annual Review of Entomology. DOI: 10.1146/
annurev-ento-011118-111923
What kinds of questions or opportunities would you hope
that young scientists will embrace in coming years in the
study of sociality and major transitions, and/or what is
missing in the field?
I hope that we move toward searching for generalizations
by examining diversity: the general rules will tell us why
species and taxa are different because of the different
situations in which they evolve and function. Instead of
looking for explanations that fit all cases, or a single
general theory, I think we will make more progress by
examining what are the ecological reasons for so many
versions of social behavior.
A basic starting point for investigating social behavior is
that it is always a response to changing conditions, and so
what we want to understand is not what animals do but
how they change what they do. The most difficult and
most fun part of designing field experiments is to find
perturbations that are large enough to generate an observ-
able response, but still within the range of changes that
the animals normally experience.
We will have to let go of the idea that each individual’s
behavior is an internal attribute, that it carries around its
behavior inside itself, like a package. Social behavior is
participation in a set of relations, with others and with the
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Insights and opportunities in insect social behavior Gadagkar et al. xiii
rest of the world. We try to break nature and nurture,
inside and outside, into separate forces, while in real life
they cannot be pried apart.
Gordon, D.M. 2015 From division of labor to collective
behavior. Behavioral Ecology and Sociobiology. DOI:
10.1007/s00265-015-2045-3
Dr Keller is a professor in the Department of Ecology and
Evolution at the University of Lausanne. His work com-
bines field and laboratory studies to examine a range of
topics in social evolution, from ageing to division of labor,
and most generally how genetic factors and social envi-
ronment shape individual behavior. His work often
focuses on the fire ant, Solenopsis invicta and the Argentine
ant Linepithema humile (and the occasional robot).
With respect to where we are in our understanding of the
evolution of social behavior, are there a couple of key
insights you had over the course of your career that you
would be willing to share?
When I started my PhD an important question was
whether the presence of several queens in the same
colony was a problem for the theory of kin selection.
My work, with that of several colleagues, showed that
polygyny is broadly compatible with kin selection, and we
also uncovered the conditions under which polygyny
should be favored by natural selection over monogyny.
Over 15 years we have thus been able to address what W.
D. Hamilton was seeing as an important issue in the field
of evolutionary biology and social behaviour.
I then got interested in unicoloniality, a process whereby
colonies contain large number of unrelated queens and
where there is no aggression between colonies. This was
seen as the next challenge for kin selection. Our work on
the Argentine ant has shown that, contrary to what had
been proposed, there had not been a change in social
organization after the ants had been introduced to the US
and Europe. Rather, we showed that the mode of social
organization of this ant is identical the native and intro-
duced ranges, the only difference being the size of the
supercolonies which are much larger in the introduced
range — probably because of decreased competition
among supercolonies and a lower pressure by parasites
and predators. Interestingly, in the native range there is
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very strong genetic differentiation among supercolonies,
and it remains an important challenge to study what
prevents gene flow between supercolonies and how
new supercolonies are formed (the Argentine ant, as many
unicolonial species does not participate in mating flights;
new colonies are formed by budding).
I have also been interested in the debate about kin
selection and group selection. Together with my col-
league Laurent Lehmann, we helped to show that con-
troversy is mostly irrelevant. Kin selection models are
formally identical to group selection models, the only
difference being the emphasis on the level of investiga-
tion (the controversy is still ongoing in part because of
confusion over the mathematical models and misreading
of previous work). Importantly, kin selection is the only
selective force that can promote the evolution of altruism
and all claims to the contrary are from studies wrongly
defining fitness or (more commonly) scientists not realiz-
ing that kin selection is operating in their model (e.g. that
their complex model leads to a situation where the agents
are interacting with clones!).
What kinds of questions or opportunities would you hope
that young scientists will embrace in coming years in the
study of sociality and major transitions, and/or what is
missing in the field?
The main question that remains is to identify the genes
involved in social behavior and the causes underlying
within-species and between-species variation. We have to
move from broad speculations to functional studies. This
definitively is not an easy task because it requires devel-
oping new genetic tools. Another problem is also that
many species cannot be bred in the laboratory, precluding
the maintenance of lines harboring specific genetic var-
iants. Another important issue will also be to determine
the extent to which supergenes are involved in underly-
ing variation in social organization. My prediction is that it
will be very frequent, just as we are realizing that many
ants have unusual modes of reproduction!
Dr Michod is a professor in the Department of Ecology
and Evolution at the University of Arizona. He studies the
principles that facilitate major evolutionary transitions
like the evolution of cooperation, sex, and multicellularity
using volvocine green algae as a model system. His work
integrates a broad range of disciplines, ranging from
mathematical modeling, ecology and molecular biology
to philosophy.
Current Opinion in Insect Science 2019, 34:ix–xx
xiv Social insects
With respect to where we are in our understanding of the
evolution of social behavior, are there a couple of key
insights you had over the course of your career that you
would be willing to share?
Our understanding of the diversity of life is being trans-
formed by the realization that evolution occurs not only
among individuals within populations, but also through the
integration of groups of individuals into new higher-level
individuals. Indeed, the major landmarks in the diversifi-
cation of life and the hierarchical organization of the living
world are consequences of a series of evolutionary transi-
tions in individuality: from genes to cooperative gene net-
works to thefirst genomeinthefirst cell, fromprokaryotic to
eukaryotic cells, from cells to multicellular organisms, from
asexual to sexual populations, and from solitary to social
organisms. It is a major challenge to understand why
(environmental selective pressures) and how (underlying
genetics, population structure, physiology and develop-
ment) the basic features of an evolutionary individual, such
as fitness heritability, indivisibility, and evolvability, shift
their reference from the old to the new level.
Why and how groups of individuals evolve into a new
kind of higher-level individual is the basic question my
colleagues and I have been working on. We have
approached this question using mathematical models,
philosophical analysis, and an experimental system —
the volvocine green algae. The basic steps of an evolu-
tionary transition in individuality, or ETI, include: (i) the
formation of groups, (ii) multilevel selection, (iii) evolu-
tion of cooperation, (iii) evolution of cheating and conflict,
(iv) evolution of conflict mediators that reduce conflict
and increase cooperation in the group, (v) evolution of
division of labor, and (vi) decoupling of group fitness from
lower-level fitness (Michod, 1999). Conflict mediators are
developmental traits that reduce the opportunity for
conflict while enhancing cooperation among group mem-
bers. Multiple organismal traits act as conflict mediators;
these traits include germ soma division of labor, pro-
grammed cell death, and genetic control of group size
(Michod, 2003). Such conflict mediators alter develop-
ment to produce groups with greater cooperation and
group-level heritability of fitness, resulting in greater
individuality of the group. In short, these modifiers
embody van Valen’s phrase that ‘evolution if the control
of development by ecology’ (van Valen, 1976).
Individuality is not a binary trait but rather comes in
grades and evolves like other traits. In a study of indi-
viduality in the volvocine algae, we showed that during an
ETI some traits underlying individuality change little
(such as genetic uniqueness or degree of spatial temporal
boundaries) while others change dramatically (traits
underlying the degree of integration and group proper-
ties) (Hanschen, Davison, Grochau-Wright, and Michod,
2017).
Current Opinion in Insect Science 2019, 34:ix–xx
During an evolutionary transition in individuality (ETI),
such as the transition from unicellular to multicellular
organisms, fitness must be reorganized, so that fitness
becomes a property of the group and not the cell (Michod,
1999, 2006, 2007). As cells specialize in the fitness com-
ponents of the group, cells lose their individual fitness,
and the fitness of the group increases. As altruism evolves,
the costs of altruism reduce fitness at the lower level while
the benefits of cooperation increase the fitness of the
group. Thus, altruism has the effect of transferring fitness
from the lower level to the level of the group. Fitness may
also be transferred from the cell level to the level of the
group by a shift in a cell property from a value optimal for
the cell to a value optimal for the group. Using this
hypothesis, we showed how reproduction could emerge
at the group level through the coevolution of a life history
trait with a trait affecting the likelihood of group forma-
tion (Maliet, Shelton, and Michod, 2015; Shelton and
Michod, 2014). As a result of these, and other processes,
fitness may be reorganized and transferred from the level
of the cell to the level of the cell group, the new multi-
cellular individual (Michod, 2005).
Responses to environmental stress provide a basis for
fitness reorganization during ETIs (Nedelcu and Michod,
2006). In the simplest formulation, fitness is the product
of survival and reproduction; these fitness components
trade-off with one another, so that, when reproduction is
delayed, survival is enhanced. Environmental stress
responses typically involve the delay of reproduction,
so that survival is enhanced through the stressful period.
Such stress responses in a unicellular organism may be co-
opted for specialization in the fitness components of the
group. Programmed cell death and delay of reproduction,
such as during cell cycle arrest, are additional stress
responses at the cell level that are likely co-opted for
the reorganization of fitness during the transition to
multicellularity.
We have tested these ideas in the volvocine green algae.
A gene which down regulates reproduction in stressful
environments in a unicellular ancestor may be co-opted to
turn off reproduction in somatic cells in a descendant
multicellular species. An example is the co-option of the
Rls1 gene in Chlamydomonas reinhardtii for somatic cell
specification in Volvox (Nedelcu and Michod, 2006).
In summary, by using the theories of fitness, fitness
reorganization, fitness trade-offs, altruism, multi-level
selection, kin selection, life history evolution, and social
evolution, we can explain using Darwinian principles a
major jump in complexity such as the evolution of mul-
ticellular organisms from unicellular ancestors. (Michod,
2007).
What kinds of questions or opportunities would you hope
that young scientists will embrace in coming years in the
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Insights and opportunities in insect social behavior Gadagkar et al. xv
study of sociality and major transitions, and/or what is
missing in the field?
I wish we better understood how group properties are
comprised out of individual properties. Early in an evo-
lutionary transition, group properties are likely aggrega-
tive properties of individual traits but new emergent
(non-aggregative) properties eventually arise. How and
why this occurs needs further study. For example, during
the transition to multicellularity in the volvocine green
algae, swimming speed of the colony is likely an aggre-
gative property of the flagellar beating of cells in the
colony. While the ratio of germ to somatic cells is an
aggregative statistic of cell properties (whether a cell is
somatic or germ), why and how cells relinquish their
individual fitness to become reproductively altruistic
somatic cells is an emergent property of interactions in
the group. Likewise, group fitness initially is an aggrega-
tive property of cell fitness, but, as the ETI proceeds and
cells specialize in fitness components of the group, group
fitness is decoupled from cell fitness.
Although I have used population genetics, game theory
and optimization theory in my mathematical work, I wish
I better understood how these approaches relate to each
other. I wish we had a theoretical or conceptual frame-
work for connecting them. For example, I have studied
the transfer of fitness from lower level cells to cell groups
using both 2-locus population genetic modifier theory and
optimization theory. Both give the same kind of general
result which gives me some confidence in its generality
(Michod, 2011). Why this should be the case, I am less
clear about. In general, we need better training in theo-
retical biology and more students with mathematical
training.
There are a number of immensely important events
without which life as we know it would be vastly differ-
ent, including such major events as the origin of the
genetic code, language, oxidative photosynthesis, and
the Cambrian explosion. Understanding these events is
critical for the field of evolutionary biology and for under-
standing life on earth. These events are not, however,
ETIs. ETIs comprise a common set of problems and
solutions involving levels-of-selection and the integration
of evolutionary units. ETIs constitute a natural kind, a
natural grouping of phenomena involving common pro-
blems and sharing common solutions. I wish we better
understood the mapping between the various processes in
the different ETIs and had a language for connecting
them (hypercycles and cooperative groups of genes to the
first genome, simple cells to complex eukaryotic cells,
single cells to multicellular organisms, solitary organisms
to eusocial societies, asexual to sexual species).
Finally, I encourage young scientists to not get swept
away by trendy topics, such as the current splash of big
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data and big science. My advice is to explore foundational
questions made specific in tractable systems that fascinate
you. Small is beautiful, especially when it comes to
research. Don’t underestimate the beauty and power of
an idea along with a framework in which to test it.
Hanschen, E. R., Davison, D. R., Grochau-Wright, Z. I.,
& Michod, R. E. (2017). Evolution of individuality: a case
study in the volvocine green algae. Philosophy Theory andPractice in Biology, 9(3).
Maliet, O., Shelton, D. E., & Michod, R. E. (2015). A
model for the origin of group reproduction during the
evolutionary transition to multicellularity. Biology Letters,11. https://doi.org/10.1098/rsbl.2015.0157
Michod, R. E. (1999). Darwinian dynamics: evolutionary
transitions in fitness and individuality. Princeton, NJ:
Princeton University Press.
Michod, R. E. (2003). Cooperation and Conflict Media-
tion during the Origin of Multicellularity from Genetic
and Cultural Evolution of Cooperation. In P. Hammer-
stein (Ed.), Genetic and Cultural Evolution of Cooperation(pp. 261–307). Cambridge, MA: The MIT Press.
Michod, R. E. (2005). On the transfer of fitness from the
cell to the multicellular organism. Biology and Philosophy,20(5), 967–987. https://doi.org/10.1007/s10539-005-9018-
2
Michod, R. E. (2006). The group covariance effect and
fitness trade-offs during evolutionary transitions in indi-
viduality. Proceedings of the National Academy of Sciences,USA, 103(24), 9113–9117. Retrieved from http://www.
pnas.org/content/103/24/9113.short
Michod, R. E. (2007). Evolution of individuality during
the transition from unicellular to multicellular life. Pro-ceedings of the National Academy of Sciences, USA, 104(Suppl.1), 8613–8618. Retrieved from http://eebweb.arizona.
edu/michod/Downloads/NAS Complexity.pdf
Michod, R. E. (2011). Evolutionary Transitions in Indi-
viduality: Multicellularity and Sex. In The Major Transi-tions in Evolution Revisited (pp. 169–197). MIT Press.
Nedelcu, A. M., & Michod, R. E. (2006). The evolution-
ary origin of an altruistic gene. Molecular Biology andEvolution, 23(8), 1460–1464. https://doi.org/10.1093/mol-
bev/msl016
Shelton, D. E., & Michod, R. E. (2014). Group Selection
and Group Adaptation During a Major Evolutionary
Transition: Insights from the Evolution of Multicellular-
ity in the Volvocine Algae. Biological Theory, 9(4), 452–
469. https://doi.org/10.1007/s13752-014-0159-x
Current Opinion in Insect Science 2019, 34:ix–xx
xvi Social insects
van Valen, L. Energy and evolution. Evol. theory. 1, 179–
229 (1976).
Dr Queller is a professor in the Department of Biology at
Washington University in St. Louis. He studies the
mechanisms underlying the evolution of cooperation.
His work combines mathematical theory with experimen-
tal biology to study conflict and cooperation in social
insects and amoebae.
With respect to where we are in our understanding of the
evolution of social behavior, are there a couple of key
insights you had over the course of your career that you
would be willing to share?
Hamilton’s insights about kin selection have driven much
of my research career. I worked out how to estimate
relatedness from genetic markers and with Joan Strass-
mann, and used that to help show that social insects are
generally highly related and that they care about related-
ness in many ways. We then showed that the same
findings apply to social amoebas. Conceptually, I have
helped frame the discussion of the benefits of sociality
(life insurance versus fortress defense) and the major
types of evolutionary transitions (fraternal versus egali-
tarian). Recently, Joan and I proposed how social evolu-
tion theory can provide us with a definition of what an
organism is.
What kinds of questions or opportunities would you hope
that young scientists will embrace in coming years in the
study of sociality and major transitions, and/or what is
missing in the field?
Social evolution theory has become a sprawling topic and
could use more efforts at unification. How do we translate
between the gene’s eye view and multi-level selection?
Do they provide us with equivalent accounts of selection?
How do we best combine kin selection and game theory?
How do we translate between models using game theory
or adaptive dynamics, inclusive fitness, population genet-
ics, and quantitative genetics? How do we make these
theoretical results useful to empirical biologists?
More empirical work needs to be done on the advantages
of sociality, including fortress defense and life insurance,
but also the role of manipulation. A particularly interest-
ing case is manipulation of social insect workers by
mothers and fathers via genomic imprinting. For the
Current Opinion in Insect Science 2019, 34:ix–xx
various major transitions, we need to better understand
the evolution of dependency and points of no return.
Dr Robinson is a professor at the Carl R. Woese Institute
for Genomic Biology and the Department of Entomology
at the University of Illinois, Champaign-Urbana. His
work combines approaches from genomics, molecular
biology, neurobiology and behavioural ecology to under-
stand the mechanisms that shape social behavior and
caste differentiation, often focusing on the honey bee,
Apis mellifera.
With respect to where we are in our understanding of the
evolution of social behavior, are there a couple of key
insights you had over the course of your career that you
would be willing to share?
I’m happy to share three. First, when I was a postdoctoral
fellow in the laboratory of Robert Page, we showed that
division of labor among workers in honey bee colonies is
influenced by heritable effects on the tendency to per-
form particular tasks. This demonstrated the kind of
genetic variation in behavior necessary to support a basic
model of the evolution of division of labor via colony-level
selection as envisioned by Darwin. We also developed a
conceptual stimulus-response threshold model to explain
the mechanistic basis of the observed genetic variation in
task-related behavior which has guided a lot of research
on social insects since.
Robinson, G.E. and R.E. Page. 1988. Genetic determina-
tion of guarding and undertaking in honey-bee colonies.
Nature 333: 356-358.
Page, R.E., Robinson, G.E., Calderone, N.W. and W.C.
Rothenbuhler. 1989. Genetic structure, division of labor,
and the evolution of insect societies. In M.D. Breed and
R.E. Page, eds., The Genetics of Social Evolution. Westview
Press, Boulder, CO. pp. 15-29.
Second, in using candidate genes and transcriptomics to
study the molecular basis of division of labor, my labora-
tory discovered that brain gene expression is highly
sensitive to social influences. In addition, when studying
colony defense, we found that some of the same genes
that respond in real-time to colony disturbance also show
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Insights and opportunities in insect social behavior Gadagkar et al. xvii
evolutionary differences in brain expression when com-
paring strains of bees that differ in levels of aggression.
Genes that act over both physiological and evolutionary
time scales provide a possible mechanism for how behav-
ioral plasticity might drive behavioral evolution through
changes in gene regulation, providing a molecular basis
for models that posit a role for phenotypic plasticity in
evolution.
Ben-Shahar, Y., Robichon, A., Sokolowski, M.B. and G.E.
Robinson. 2002. Influence of gene action across different
time scales on behavior. Science 296: 741-744.
Whitfield, C.W., Cziko, A.-M. and G.E. Robinson.
2003. Gene expression patterns in the brain predict
behavior in individual honey bees. Science 302: 296-299.
Alaux, C., Sinha, S., Hasadsri, L., Hunt, G.J., Guzman-
Novoa, E., DeGrandi-Hoffman, G., Uribe-Rubio, J.L.,
Rodriguez-Zas, S. and G.E. Robinson. 2009. Honey bee
aggression supports a link between gene regulation and
behavioral evolution. Proceedings of the National Academy ofSciences 106: 15400-15405.
Third, relying on large-scale sequencing of transcrip-
tomes and genomes across different species of bees,
and in collaboration with several other labs, my laboratory
discovered that the evolution of eusociality involved an
increase in the complexity of gene regulatory networks.
Some of the key regulatory processes involved are meth-
ylation and interactions between transcription factors and
their binding sites, acting on a variety of biological pro-
cesses including metabolism and hormone signaling.
Similar results have been reported for ants, suggesting
that these evolutionary insights are robust and reflect
remarkable convergence.
Kapheim, K.M, G.E. Robinson. 2015. Genomic signa-
tures of evolutionary transitions from solitary to group
living. Science 348: 1139-1143.
Woodard, S.H., Fischman, B.J., Venkat, A., Hudson, M.
E., Varala, K., Cameron, S.A., Clark, A.G. and G.E.
Robinson. 2011. Genes involved in convergent evolution
of eusociality in bees. Proceedings of the National Academy ofSciences 108(18): 7472-7477.
What kinds of questions or opportunities would you hope
that young scientists will embrace in coming years in the
study of sociality and major transitions, and/or what is
missing in the field?
Sociogenomics is still a young science, and there is much
to do. More genome sequencing — more species, more
individuals within species, and new analytics to handle
unprecedented amounts of sequence data — will enhance
our ability to use social insects as models to address
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important questions at all levels of biological organization.
Improved tools to manipulate genes and genomes,
together with continued development of automated
behavioral monitoring technologies in social insect colo-
nies, will deepen our understanding of the causal relation-
ships between genes and social behavior. And further
development of models of gene regulatory networks,
integrating different types of’ omics data, especially from
the brain, will provide the foundation for a better under-
standing of how genes work together to orchestrate neural
and behavioral plasticity.
Chandrasekaran, S., Ament, S.A., Eddy, J., Rodriguez-
Zas, S., Schatz, B.R., Price, N.D. and G.E. Robinson.
2011. Behavior-specific changes in transcriptional mod-
ules lead to distinct and predictable neurogenomic states.
Proceedings of the National Academy of Sciences 108: 18020-
18025.
Gernat, T., Rao, V.O., Middendorf, M., Dankowicz, H.,
Goldenfeld, N.D. and G.E. Robinson. 2018. Rapid and
robust spreading dynamics despite bursty interaction
patterns in honey bee social networks. Proceedings of theNational Academy of Sciences 115: 1433–1438.
Lewin, H.A., Robinson, G.E. W.J. Kress . . . G. Zhang.
2018. Earth BioGenome Project: Sequencing life for the
future of life. PNAS 115: 4325-4333.
Dr Strassmann is a professor in the Department of Biol-
ogy at Washington University in St. Louis. She studies
how cooperative behaviors are maintained despite exten-
sive individual conflict. Her research on altruistic beha-
viors includes studies of cooperation in both paper wasps
and social amoebas.
With respect to where we are in our understanding of the
evolution of social behavior, are there a couple of key
insights you had over the course of your career that you
would be willing to share?
Sociality with altruism, individuals that give up their
reproduction to help rear others, has only happened in
one way in social insects, when young stay with their
parents to help raise siblings. There are other forms of
sociality in social insects that are founded on selfish herd
principles and the aggregative nesting of various wasps
Current Opinion in Insect Science 2019, 34:ix–xx
xviii Social insects
and bees, but these have never led to within-colony
altruism.
For research, a key insight is that important results come
from careful field work of marked individuals on video-
taped colonies where genetic relatedness among inter-
actants is then measured. Work on multiple species to
avoid the blinders one species can instill.
Hamilton’s Rule is a powerful guide for research on social
insect conflicts of interest. Genetic relatedness within
wasp colonies is generally high, between 0.3 and 0.75,
though not as high as it would be among workers with a
single, once-mated mother. This is largely because of
queen turnover, or multiple queens in the Polistine
wasps. Relatedness asymmetries correctly predict con-
flicts of interest in sex ratio and in who produces the
males.
Social insects recognize colony members and do not
discriminate within colonies.
In Polistes wasps, the queen is not a pacemaker. She does
not orchestrate worker behavior, or take a colony from
inactive to active, but she does move actively over the
nest rubbing pheromones. In early colonies of multiple
queens and no workers, clear dominance behavior by the
queen occurs. In epiponine swarm-founding wasps like
Parachartergus, the queens are very specialized as egg
layers, often staying in the back of the nest and darting
to empty cells to lay eggs, then retreating. Clearly the
transition to queen as egg layer rather than boss happens
early.
Genetic conflicts of interest are clear in social insects. In
Polistes, protogeny, the production of females before
males at the end of the colony cycle, lets the divide
between workers and queens happen more flexibly and
increases worker control. Tropical swarm-founding
wasps, Old World and New World, have cyclical oligo-
gyny, a kind of split sex ratios where worker interests push
queen production to colonies with the fewest existing
queens, and male production to those with multiple
queens in a striking case of convergent evolution.
It is easier to measure relatedness than costs and benefits
of social interactions. In stingless bees, workers varied
among species in their tendency to produce the males
themselves, though worker to brood relatedness was
similar across those species. This is likely to be because
of differences in costs and benefits of these actions, but
exactly how so is hard to figure out.
What kinds of questions or opportunities would you hope
that young scientists will embrace in coming years in the
study of sociality and major transitions, and/or what is
missing in the field?
Current Opinion in Insect Science 2019, 34:ix–xx
To understand major transitions in social evolution, it is
good to study organisms that bridge a transition. This
might be single species as they grow larger in group size,
or multiple species on a phylogeny that encompass the
transition being studied. An important transition in
insects is that from solitary to social. What changes
between solitary or nearly solitary species and social
species as they become more social? Halictine bees,
Polistes wasps, and Stenogastrine wasps come to mind
for such studies. Polistes biglumis in the Alps produces few
or no workers. Sticking within the same sub genus, Polistesdominula can have colonies of hundreds. How has the role
of the main egg layer changed? What are the changes in
gene expression; how has selection operated on those
genes; are there meaningful differences in pathways that
make sense?
Some social insects have a solitary developmental stage
while others do not. What changes during development?
This does not match caste differences necessarily. For
example, fungus growing ants have a solitary stage where
a single queen begins her colony and fungus garden,
feeding the tiny first workers trophic eggs and fungus.
She will ultimately have a colony of millions. The epi-
ponine wasps by contrast, never have a solitary stage since
they are swarming, but they never develop physical castes
in most species either. Is this a constraint because workers
fly?
Observational studies of worker and queen behavior
using modern marking techniques (barcodes and radio-
tagging) and videotaping along with judicious experimen-
tation have been underused in field studies of wasps to
understand where power lies.
Ants have developed unicoloniality, the loss of kin rec-
ognition and family structure which has led to colonies of
billions spreading across the landscape. How has this
happened? Has it resulted in the decay of worker traits
since natural selection cannot work on them anymore?
We reviewed this field some time ago (Helantera et al.2009). What has changed?
There are some other crazy things going on genetically in
ants. Pogonomyrmex ants that produce workers only from
sperm coming from different species. Wasmannia that
have males and females from different clones with no
contribution from the other parent. How about clonality
in Vollenhovia? Have all these genetic mechanisms been
reviewed lately? Can we do more large-scale screens for
them? What do they tell us about the maintenance of
sociality and the integrity of genomes in ants? Do these
kinds of things occur in other social insects?
Within colony conflicts of interest need to be controlled in
an organism. If a social insect colony is an organism, how
are these conflicts controlled? What conflicts remain?
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Insights and opportunities in insect social behavior Gadagkar et al. xix
These are questions that were studied a lot some time ago
and have been largely forgotten, but they are not
answered. Stingless bees are particularly intriguing.
How can we better use the information from whole social
insect genomes and transcriptomes? So far, these
approaches are very preliminary. What can we really
learn? When will information from genomics be better
meshed with behavior, development, and ecology?
Dr West-Eberhard is a researcher at the Smithsonian
Tropical Research Institute and the Escuela de Biologia
at the University of Costa Rica. Her work examines the
role of phenotypic and developmental plasticity in the
evolution of behavior. She studies the evolution and
behavior evolution of social wasps.
Here are some brief responses to the two questions I was
asked by the editors. First: “With respect to the evolution
of social behavior, what are some key insights you had
over the course of your career?
I will take ‘key insights’ to mean things that changed my
thinking relative to what I thought before, and to the
impressions given by much of the literature at the time.
On kin selection: Hamilton’s Rule as a behavioral deci-
sion rule, with dominance rank an estimator of benefit vs
cost (K).
Hamilton’s 1964 papers came out while I was a graduate
student, in the field in Cali, Colombia, studying
Polistes. Hamilton mentioned many organisms, including
Polistes, which he had observed in Brazil. But he, and
discussions by others, strongly emphasized the theoretical
importance of genetic relatedness; and the theory was
formulated in terms of population genetics. The behavior
of ‘my wasps’ indicated that they were sorting themselves
into groups of relatives where subordinates helped (as
workers) others — dominants (reproductives) — they
behaved as if they were using phenotypic aggressiveness
as an estimator of relative reproductive value (ovary size,
which correlated with degree of aggressiveness). In other
words, they seemed to evaluate the cost/benefit ratio (K)
of Hamilton’s rule, while at the same time staying in
groups with high relatedness (r). So I saw ‘Hamilton’s
Rule’ (K > 1/r) not in terms of population genetics but as a
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decision rule used by individuals to behave in ways that
would raise their inclusive fitness. That was an important
insight for me and I think that my thesis publications (e.g.
Science 1967) were the first to examine kin selection
theory with quantitative field data. I believe that kin
selection ideas achieved the prominence they did not
because of their impact on population genetics, but
because scientists working on social behavior did as I
did — used Hamilton’s Rule as a decision rule to predict
when ‘altruism’ (beneficent behavior costly to production
of own offspring) would occur.
Mutualism and eusociality
Initially I was such a thoroughgoing kin-selectionist that I
did not really believe a claim by Charles Michener about
bees — that mutualistic groups could give rise to eusoci-
ality (worker behavior, beneficial to others while costly to
the performer). However, the tropical wasp Metapolybiaaztecoides enabled me to understand Michener’s insight
about mutualism. Dominant queens in newly founded,
vulnerable (to predation) colonies produced only workers
— they were mutualistic in that all contributed sterile
daughters to the group, and although they engaged in
aggressive displays, refrained from strong competition.
But later, when the colony was larger and less vulnerable,
they abandoned mutualistic cooperation and became
extremely aggressive until only one eventually prevailed,
with some former egg-layers becoming workers and some
leaving the colony. This, essentially, was what Michener
had seen in less specialized groups of bees, whose mutu-
alistic beginnings led eventually to worker-containing
groups.
Parallels between competition in social groups and com-
petition for mates (sexual selection)
Early in my career I also thought that the only true
sociality, in a special class by itself, was sociality that
occurred within social groups. I put aside, in my own
mind, mating behavior as another kind of interaction.
This was partly because when I was a student mating
behavior was seen by evolutionary biologists mainly in
the context of speciation and isolating mechanisms. But
this was changed, again, by an insight seeded by someone
else, this time unpublished and oddly expressed. After a
talk I gave at a big congress, describing social displays of
wasps, a psychologist named Nicholas Thompson came
up to me and said: “Don’t you think that social behavior is
like sexual selection?” and he went on to say that both
involve ‘fads.’ At first I had no idea what he was talking
about, but he convinced me of an essential similarity
between the competitive displays of wasps and those of
male peacocks and fighting stags: all employ behaviors
and morphologies that are like ‘fads’ in contributing, like
a trendy hairdo or the latest style of dress, to social status,
not survival or ecological success. This developed into a
Current Opinion in Insect Science 2019, 34:ix–xx
xx Social insects
broader insight, pinpointing the special aspects of ‘social
selection’ in both contexts, and how it is distinctive, as
had been argued by Darwin for mating behavior, when he
set sexual selection apart from natural selection (the
theme of the Origin) for special treatment in a separate
book. I developed this insight in papers on speciation and
‘social selection.’
Conditional alternative phenotypes as models of flexible
development in relation to evolution
Sexual selection, social and competition within groups,
and intraspecific ecological competition, result in condi-
tion-sensitive alternative phenotypes that can become
highly specialized morphologies, physiologies, and beha-
viors — workers and queens are just one example. This
led me to think about how these, being independently
expressed and independently subject to selection, can
come to characterize different species; and how they
relate to traits within individuals, where branching devel-
opment produces semi-independently evolving ‘traits.’
Ultimately, this set of insights led to a book on Develop-mental Plasticity and Evoluton.
All of my contributions to these ‘insights,’ if I may glorify
them with that term, came from studying social insects.
All began early — during graduate school and the ensuing
ten years. And all are related to what is evidently a theme
of this special issue — major transitions in evolution. In
social insects, competition leads to alternative pheno-
types (workers and queens), which happen to be
‘dependent’ alternative morphs — the more specialized
they become the less they are able to exist in isolation,
one from the other. This contributes to the strength of
selection at a new level — the level of the group. But it
remains important to attend to signs of competition
within groups, and to recognize multiple levels of selec-
tion. Similarly, to understand adaptive evolution in gen-
eral you have to visualize selection at different levels,
with individual fitness composed of the fitness effects of
the different ‘traits’ that compose an individual. To the
degree that a ‘trait’ is underlain be particular sets of
expressed genes it is semi-independently subject to
selection
I guess the point of ruminating about these insights
relates to the second question I was asked to address: –
“What kinds of questions or opportunities would you
hope that young scientists will embrace in coming years
in the study of sociality and major transitions, and/or what
is missing in the field?”
Current Opinion in Insect Science 2019, 34:ix–xx
Social insects have long inspired generalizations in biol-
ogy, but there are two things in their study that have paid
off for me and are now rather rare. One is an early
resolution about how to do research. My aim was to
become an expert about a taxon, namely social wasps
— to learn everything known about them from systemat-
ics to physiology and behavior, and to observe them
closely myself, especially in natural settings. The second
was to look for the broader significance of what I learned.
That is: I did not set out to test hypotheses invented by
other people. Sometimes my data could be used to do
that, as in the case of kin selection ideas, but beginning
with the organisms meant seeing that theory differently
than many others did: I could see that there was more to
the story than genetic relatedness alone. That — begin-
ning with particular organisms —automatically lends
some originality to a contribution, as well as serving as
a kind of ‘power base’ in real-life facts. If you deeply
understand an organism or a taxonomic group you have a
foothold for reflecting critically on all kids of ideas,
bouncing them off what you know to be true about a
group.
What is missing in social insect research? I think that what
is increasingly missing is people doing fieldwork on
behavior and natural history. Not only is fieldwork enter-
taining, but it stimulates curiosity-driven research, and
produces revealing facts, about function and adaptive
evolution. I think this decline in fieldwork is partly
due to pressure to run a lab that can qualify for big grants.
And it is also true that lab work is now necessary to answer
may of the questions about condition-sensitive develop-
ment, gene expression, and hormonal physiology that are
important for understanding social insect evolution. The
solution is obvious — to look for ways to combine labora-
tory research with behavioral observations.
The future of evolutionary biology looks promising for
that kind of combined research. For a time, the field was
preoccupied with transmission genetics and progress in
molecular biology focused on DNA. Now genetic
research is moving toward the phenotype, symptomized
by terms like ‘proteomics’ and ‘epigenetics’ and other
indicators of emphasis on gene expression and environ-
mental influence rather than transmission genetics alone.
A focus on gene expression means thinking about the
genes that actually underlie particular evolved traits. As a
result, it becomes increasingly relevant to know what
those genes actually do, with respect to behavior, physi-
ology and morphology. And that boils down to a return to
the field, where the traits actually influence selection.
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