Insights and opportunities in insect social behaviorces.iisc.ac.in/hpg/ragh/cv/Gadagkar_Publications/... · Insights and opportunities in insect social behavior Raghavendra Gadagkar,

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

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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


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

www.sciencedirect.com

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.


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?


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.


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





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


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).





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


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!).





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.


xiv Social insects





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).


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).




Insights and opportunities in insect social behavior Gadagkar et al. xv



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


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

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transitions in fitness and individuality. Princeton, NJ:

Princeton University Press.

Michod, R. E. (2003). Cooperation and Conflict Media-

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cell to the multicellular organism. Biology and Philosophy,20(5), 967–987. https://doi.org/10.1007/s10539-005-9018-

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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.





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.





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


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.





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


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.





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


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.





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


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.






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?


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


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


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?”


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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