The evolution of insect societies

The evolution of insect societies Robert E. Page, Jr

The organization and evolution of insect societies has amazed natural historians since Aristotle. Charles Darwin considered social insects to be a major difficulty for his theory of evolution by natural selection because they demonstrate a rich diversity of adaptation among sterile workers leading to a complex division of labour, something that should not occur if variation in individual reproductive success is the grist for the mill of natural selection. This article shows how division of labour can self-organize from groups of cohabiting individuals without the necessity of a past history of natural selection for co-operative behaviour. It then explores how more complex social systems may evolve.

The organization of insect colonies is truly one of the marvels of the natural world. But to Darwin [l], the social insects presented three major difficulties for his fledgling theory of evolution by natural selection. The first difficulty was the occurrence of sterile workers in colonies, which was difficult to explain with a theory that focused on the survival and reproductive success of individuals. The second difficulty he considered to be even more serious, the divergence in characters between the reproductive queens and the non-reproductive workers. How could workers evolve characters when they do not reproduce? But he considered the most serious difficulty to be the differenti- ation among workers for anatomical traits and behaviour. Darwin’s first difficulty, the evolution of a sterile worker caste, has received by far the most attention over the past 30 years [2,3]; however, relatively little attention has been paid to how workers and insect societies evolve.

Here, I will focus on Darwin’s second and third difficulties, specifically on the evolution of worker behaviour that is the basis of the evolution of insect societies. I will begin by exploring the origins of division of labour. I will show that division of labour is not difficult to explain; in fact it seems to be an inescapable property of group living. Then. I will make a giant leao forward to

I

explore the evolution of the highly complex societies of honey bees, one of the most complex among the social insects. I will argue that the same inescapable properties of group living that give rise to rudimentary division of labour provide the substrate for building more complex societies. And, finally, I will present the results of an artifi- cial selection programme designed to identify selectable colony-level ontogenic

Robert E. Page, Jr

Is a professor in the Department of Entomology, University of California, Davis. His research inter- ests have always been in the genetical aspects of the evolution of insect social behaviour. For the past IO years his work has focused on the foraging behaviour of honey bees.

114 Endeavour Vol. 21(3) 1997

(sociogenic) pathways leading from genes to colony phenotypes. I will show how colony-level selection applied to a colony phenotype results in the substitution of alleles at specific genes contained in mapped genomic regions within workers. Then I will trace the effects of these genes back through individual worker behaviour to the colony phenotype.

Origins of division of labour How did social organization with a pronounced division of labour, such as that found in social insects, evolve? To answer this question we must first explore its origins. I believe that at least the rudiments of division of labour are inescapable properties of groups. There never was a time in the history of the evolution of social insects where individuals shared nests and did not have a division of labour. This is a consequence of two processes that facilitate and place con- straints on the evolution of social organization: the stimulus-response relationship of neurophysiology, and the correlation between a behavioural response and the stimulus that induced it.

Stimulus-response relationships The working model of animal behaviour assumes that individuals respond to stimuli that they perceive in their environment. Each behavioural response is conditional on the relationship between the strength of the stimulus (or stimuli) and the response threshold of the individual. This is a consequence of neurophysiological processes at all levels: sensory perception and inte- gration, and motor response. Neurons either fire an electrical impulse or they do not. Individuals either perform a behavioural act or they do not. Response thresholds can vary among individuals due to differences in physiological state, experience, genotype, etc. For example (Figure l(a)), honey bee workers respond to sugar-water stimu- lation of the antenna by extending their tongue (proboscis). ‘Hungry’ bees respond with a higher frequency and to lower concentrations of sugar than they do after they

have been fed (R.E. Page and J. Erber, unpublished data). In other words, hungry bees have lower response thresholds.

Response-stimulus correlations There may also be a correlation between the stimulus that results in a behavioural response and the behavioural act itself. For example, honey bees remove dead bodies from the nest [3]. So-called ‘undertaker’ bees drag the bodies of their dead nestmates from the nest (Figure l(b)), then fly away with them and drop them at some distance from the colony. The dead bee is a stimulus that releases the set of behavioural acts resulting in the performance of the removal task and by that action other workers with higher response thresholds are prevented from performing that behavioural act - a division of labour. Individuals with lower response thresholds to dead-bee stimuli may respond with a higher probability, or more rapidly, than those with higher response thresholds. The stimulus level for undertak- ing behaviour is decreased by the behavioural act because the stimulus, the dead bee, is removed by the act. By responding, they remove the dead-bee stimulus.

Individuals presumably have different response thresholds associated with many different stimuli associated with many different tasks. For instance, individuals may vary for response thresholds for temperature associated with thermoregulating behaviour, or response thresholds to chemicals released by workers that are associated with defensive behaviour. Variation in the collective sets of response thresholds should result in the observed colony-level patterns of division of labour.

Examples of spontaneous division of labour Ceratina flavipes Division of labour occurs spontaneously even among individuals of strictly solitary species when they are induced to cohabit. Ceratina flavipes is a small, solitary-nesting carpenter bee found in Japan. Females construct their nests independently by boring

Copyright 0 1997 Elsevier Science Ltd. All right reserved. 0160-9327/97/$17.00. PII: SO160-9327(97)0103

03

Figure 1 (a) The proboscis extension reflex of the honey bee. A worker honey bee is restrained in a small brass tube. A droplet of sucrose solution is applied to the tip of one antenna and the proboscis is extended. (Photograph by Joachim Erber.) (b) An ‘undertaker’ bee dragging the body of a dead nestmate out of the entrance of a colony. (Photograph by Francis Ratnieks.)

out the centres of plant stems. They then forage for pollen and nectar from which they make a food mass similar to a loaf of bread on which they lay a single egg that will hatch, devour the pollen loaf, and develop into an adult. Sakagami and Maeta [4] examined 2307 natural nests and found only three that contained more than one adult female - they each had just two - demonstrating a high degree of intolerance of nest-sharing in this species. They were able to ‘coerce’ five pairs of females to suc- cessfully co-found nests by placing them together in a cage with a single nest site. In every case, a reproductive division of labour was established, with one individual laying eggs and guarding the entrance while the other did most of the foraging. Thus, a task and reproductive divi&on emerged from the association mally intolerant individuals.

of labour of two nor-

Pogonomyrmex barbatus Behavioural differences also occur when queens of the desert ant, Pogonomyrmex barbatus, are coerced to co-found nests. Like most species of ants, P. barbatus queens found nests by excavating a cham- ber beneath the surface of the ground where they lay eggs and raise a first batch of workers from glandular secretions derived from their own body reserves. After the first workers develop into adults, the nest is opened and only the workers forage above ground. Extensive studies of p barbatus populations have found them to have only single foundress nests (Robert Johnson, per- sonal communication), like all other species in this species complex.

Jennifer Fewell (J. Fewell and R. Page, unpublished) forced 31 pairs of young queens into foundress associations by placing them together in glass vials containing

sand. Queens jointly excavated nests but a pronounced division of labour emerged in nearly every case with one foundress doing a significant majority of the digging. Also, in nearly every case, the nest excavating specialist died first, before the emergence of the first adult workers, thus resulting in a task and reproductive division of labour. Queens in some pairs were tested as solitary diggers before they were combined. There was significant variation observed among queens. In every paired case the queen that spent more time digging as a solitary foundress also dug the most as a CO- foundress. However, the differences between the co-founding queens were greatly amplified when sharing a nest, demonstrating that not only does natural variability exist for digging behaviour but also that sharing a common environment can increase those differences into a pronounced division of labour (see also [5]).

Evolution of complex social behaviour How do complex insect societies evolve? The main features of insect societies that attract our attention and awe are consequences of interactions among colony members and between colony members and their environment, characters that are far removed from the units of selection, the genes. Insect colonies have no single social genotype as a unit of evolutionary change. Instead, the genotype of a colony is distrib- uted among sometimes thousands of geneti- cally unique individual workers. Natural selection acts on existing heritable variation to effect evolutionary change. So, if natural selection is the designing agent of insect societies, what are the characters that vary and are subject to evolutionary change, how are they inherited, and how do the changes that occur result in the variety of organizational patterns that we observe? I will answer these questions by focusing on the evolution of honey bee societies, beginning with a brief discussion of their natural history.

Natural history of honey bees Colonies of honey bees construct their nests in cavities (see [6] for a review of honey bee natural history). Nests are composed of wax combs that contain thousands of individual hexagonal cells that serve as the receptacles for stored food and for raising new bees (the brood). Honey, pollen and brood are segre- gated into specific regions of the nest. Although combs are oriented vertically, and lie parallel to each other, one can think of the brood nest as organized into three con- centric hemispheres, with brood in the centre, surrounded by a layer of pollen and honey to the sides and top. So, if one were to remove a single comb from near the centre of the nest it would contain brood, pollen and honey (Figure 2(a)). A honey bee colony is normally composed of a single reproductive queen, 10,000-40,000 normally non-reproductive workers, and none

Endeavour Vol. 21(3) 1997 115

(4

(b)

Figure 2. (a) A wax comb removed from near the centre of a commercial honey bee nest. When housed in commercial hives, honey bees construct their wax combs inside wooden frames that facilitate removal and inspection. This comb demonstrates the spatial relationships of honey (upper and outer edges), pollen (the semicircular band with yellow pollen in the cells), and brood (the cells in the centre of the comb with brown cappings). (Photograph by Kim Fondrk.) (b) A foraging honey bee collecting pollen from an almond blossom. (Photograph by Kenneth Lorenzen.)

to several thousand males (drones), depend- ing on the time of year. Worker honey bees are females that are derived from fertilized eggs and perform almost all of the tasks necessary for the nutrition, defence and reproduction of the colony. Colonies have a division of labour among workers that usu- ally correlates with age. As bees age, their task performance probabilities change. For example, very young bees often clean the wax cells in which worker and drone larvae are raised, and feed the brood. During their second or third weeks of life workers usu- ally make a transition from working in the nest to foraging outside for food, water and building materials (propolis, a resinous plant product). Food foragers collect pollen (Figure 2(b)), nectar, or both pollen and nectar. Once they begin foraging they are seldom observed performing tasks within

the hive, such as feeding the brood. They live for about six weeks during the active foraging time of the year.

A colony phenotype To understand how social organization evolves, we must first have a concept for a colony phenotype. The phenotype of an individual organism consists of its observ- able characteristics that result from its genetic composition (its genotype) and its environment. One way to define a colony phenotype would be to describe the behavioural state of a colony. For example, we could make a list of what each individual in the colony is doing at some instant in time. Or, make a list of all the different behavioural acts that honey bee workers perform and take an instantaneous count of the numbers of individuals engaged in each act, and

so on. Alternatively, and more realistically, we could measure the consequences of the activities of groups of task-performing workers. For example, we could measure the quantities of stored honey, pollen and immature bees as consequences of the activities of workers engaging in the behavioural acts of foraging for nectar and pollen, and feeding developing larval bees.

Pollen hoarding Pollen hoarding, the storing of surplus pollen, is a particularly interesting and complex colony phenotype. Quantities of stored pollen are the result of two processes: the rate at which pollen is brought into the colony by foragers, and the consumption of pollen by nurse bees that convert the pollen proteins into glandular secretions fed to developing larvae [7]. Pollen hoarding is an ideal trait to study because: (1) pollen is stored in specific areas, making it easy to measure, and (2) it is regulated by honey bee colonies, giving it high measurement repeatability. When additional stored pollen is added to a colony, workers reduce their foraging effort for pollen by switching to nectar foraging, or they reduce their foraging rate (the number of trips per unit time) and reduce the size of the loads they carry [8,9]. This continues until they consume the excess pollen to near the amount contained before the manipulation. The opposite holds when stored pollen is removed. Workers switch to pollen collecting, or increase their pollen foraging rates and load sizes until they again obtain their premanipulated storage level.

A network model of pollen-foraging decisions We can depict the foraging behaviour of a colony as an informational network with three components: N, the number of elements in the network; K, the connected- ness of the network, the information that each element has about the status of other elements in the net; and F, the set of decision functions expressed by the elements [lo]. Figure 3(a) shows a net with five elements each with complete information of the status (on or ofl of all other elements in the net. Each element itself can execute a decision to be on or off on the basis of the status of the others. For example, the elements may be foragers and the decision is whether to forage for pollen. An individual that makes the decision to forage for pollen is on and conveys that information, via the directed arrows, to all other foragers. The decision rule could be ‘forage for pollen if there are fewer than three other pollen foragers’. This would be a threshold-type function.

Honey bee colonies consist of several thousand foragers, they have a very large N, so it is unlikely that they get their information in this direct way. However, foragers are informationally connected by sharing common stimuli in the nest. Although we do not know what the stimuli are, they are


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Figure 3 (a) A diagrammatic representation of an informational network containing five elements (grey dots) each receiving information about the status of all other elements (incoming arrows) and each sending out information about its status to all other elements (outgoing arrows). (b) A diagrammatic representation of a model pollen foraging network. The illustrative ‘comb before’ on the left has nine empty cells (shown by open circles; the solid circles represent cells filled with pollen). The response threshold functions of two individuals (potential pollen foragers) are shown in the middle as f, and f9. The individual with the threshold function f, responds because the stimulus exceeds her response threshold. She then fills one cell, marked in grey, changing the stimulus environment represented by the ‘comb after’. Individual f, does not respond because her response threshold is not exceeded by the stimulus level. By continuing to respond whenever cells are emptied by consumption of pollen, individual f, will effectively block out individual f9 from pollen-foraging behaviour.

clearly related to the amount of stored pollen, and honey bees do behave as though they exercise threshold-type decision rules for pollen foraging based on the quantity of pollen [ll]. Therefore, we can build a some- what more realistic, illustrative model based on the network concept and on the biology presented.

Colonies consume pollen at a rate depen- dent on the amount of young larvae that are being fed. Foragers collect pollen and store it in cells; therefore, the amount of pollen stored in the comb represents the collective efforts of the pollen foragers in response to the need of the colony. Assume that empty cells in the pollen storage region of the brood nest is a stimulus (or is directly related to a stimulus) that releases pollen foraging behaviour, or alternatively, filled cells inhibit pollen foraging. Then, as pollen consumption increases, the number of empty cells will increase, resulting in an increase in the pollen foraging stimulus, or a decrease in the inhibition.

Assume that different foragers have different response thresholds with respect to how many empty cells they need to encounter before they turn on or off to pollen foraging (Figure 3(b)). These differences could be a consequence of having different genotypes, being of different ageibehavioural states, or differences in pre- or post-foraging experience. Once they respond, they fill a cell and alter the stimulus environment, thereby decreasing the likelihood that other individuals with higher response thresholds will forage for pollen. Therefore, individual foragers are informationally connected through the foraging record provided by the pollen stored in the comb. Computer simulations have shown that, with these conditions - variation in response thresholds and a correlation between response thresholds and the stimulus environment - a strong division of labour will emerge as a self-organized property of the group [lo]. Also, the stimulus environment - the quantity of stored pollen

_ will reach a regulated equilibrium that is determined by the distribution of response thresholds of the workers.

Natural selection cannot ‘see’ all of the intricate and complex interactions within a colony, nor is it likely that the genome can orchestrate them. Instead, natural selection must act on colony-level organizational components that through self-organizing processes result in specific complex behavioural patterns. These colony-level organizational components are N, K and F, where for the pollen hoarding colony level trait, N = the number of individuals competent to forage for pollen, K = the informational architecture associated with relevant pollen- foraging stimuli, and F = the set of response thresholds of the N foraging individuals to the relevant pollen-foraging stimuli.

Pathways from genes to colony phenotype In order to understand how selection results in changes in social organization, we need to identify pathways from genes to colony phenotypes. Colony-level selection operates at the level of the colony phenotype but changes the population frequencies of genes that reside in individuals: queens, workers and drones. Pathways consist of three levels that, together with developmental processes that join them, define the ontogeny of a colony-level trait. Changes at any of these levels can result in a change in the colony phenotype (Figure 4).

The first level is that of the genome. Allelic substitutions occur as a consequence of selection and result in changes of gene action, gene interaction, and the numbers and recombination rates of variable genes responsible for genetic variation of the trait. Next is the process of individual behavioural development. This includes ontogeny from egg to adult and behavioural developmental processes that are a consequence of age and experience. Variation at the individual level results from genetic variation and variation in developmental processes. Individual variation that affects patterns of social organization can be grouped into behaviour, life history and anatomy. These groupings are not necessarily independent. Individual variation affects the colony-level organizational parameters N, K and F which through self-organized colony-level developmental processes result in the colony phenotype. The self-organizing processes are a consequence of the stimulus-response threshold relationships and the correlation between the response and the stimulus environment. This is the same mechanism as described above for the case of two individuals co-habiting.

Selecting for pollen hoarding Kim Fondrk and 1 conducted a selection programme designed to identify selectable pathways from genes to colony phenotypes and to determine specifically which pathways were affected by selection for pollen hoarding [12]. Two-way selection was per- formed on a single trait, the amount of


Genome - gene action gene interaction gene number recombination

Colony H - Development - Colony (N) number stimulus-response-threshold (K) information response-stimuluscorrelation

phenotype (F) threshold set

Figure 4 The sociogenic pathway from genes to colony phenotype.

pollen stored in combs of colonies. The high and low strains diverged very rapidly. After a single generation of selection they differed significantly for the average amount of stored pollen. After three generations, colonies from the high-pollen-hoarding strain contained an average of about five times more pollen than did colonies of the low-pollen-hoarding strain. These results demonstrate how selection can result in change of a complex phenotypic trait that involves the action and interaction of a large number of genotypically heterogeneous individuals.

Colony-level mechanisms In each generation we measured several colony traits that could possibly affect the stored-pollen colony phenotype. These are plausible mechanisms in the gene-to-phenotype pathway. For example, selection could increase the number of pollen foragers, thus increasing the intake rate of pollen relative to consumption. Or, selection could reduce consumption by having fewer larvae but workers that live longer, and so on. We found genetic variability for several traits, but only one -the proportion of the foraging population that collected pollen - demonstrated a significant selection response.

We counted returning pollen and nectar foragers at the entrances of colonies. The average number of returning foragers was the same in both strains, but their ratios of pollen and nectar foragers were very different. Selection resulted in an increase in pollen foragers in high-pollen-hoarding strain colonies and an increase in nectar foragers in colonies of the low-pollen-hoarding strain, but no change in the total number of foragers. These results demonstrate that pollen and nectar collection negatively co- vary, suggesting a common genetic control for foraging behaviour, and that the allocation of foragers into pollen and nectar foraging tasks is a selectable colony-level mechanism.

Individual-level mechanisms We also studied many individual-level traits as plausible mechanisms affecting quantities of stored pollen. We found that selection for quantities of stored pollen resulted in changes in workers in their response to pollen-foraging stimuli. High-strain foragers were more likely to be observed collecting


pollen than were foragers from the low strain [13]. Low-strain workers were more likely to collect nectar. These results demonstrate a selectable individual-level mechanism, foraging resource choice, that is the cause of the colony-level mechanism, the allocation of foragers for pollen and nectar collecting.

At the sensory-physiological level, foragers that collect pollen demonstrate different response thresholds to sugar solutions and water (R.E. Page, J. Erber and M.K. Fondrk, unpublished) compared with foragers that do not collect pollen (presumably collecting nectar and water). Nectar consists primarily of dissolved sugars. Response thresholds were tested by capturing returning foragers, restraining them in small brass tubes (see Figure l(a)), then repeat- edly touching the tips of their antennae with sugar solutions of increasing concentrations. A forager would respond by extending her proboscis (tongue) when the concen- tration of sucrose exceeded her response threshold. Pollen foragers had lower response thresholds than nectar foragers and responded more often to pure water.

When we compared foragers from our high- and low-pollen-hoarding strains that were raised in a common colony, we found the same relationship between returning high-strain nectar and pollen foragers. However, we also found that high-strain liquid (nectar and water) foragers had lower response thresholds to water and sucrose than did low-strain liquid foragers - they were more like pollen foragers. These differences were also apparent between depart- ing foragers of the high and low strain and correlated with the liquid materials that they collected. High-strain liquid foragers were more likely to collect water and nectar with lower concentrations of sugar than were the low-strain liquid foragers. This suggests that our colony level selection changed the response thresholds of foragers to sucrose and water which in turn affected the kinds of materials they collect.

The genome Genetic linkage-map studies have revealed regions of the honey bee genome that affect the amount of pollen stored in the comb and foraging decisions of workers [13-151. We constructed a linkage map of the honey bee genome from males derived from a queen that was a hybrid

between the high- and low-pollen-hoarding strains. Males are haploid (have just one set of chromosomes) and are derived directly from eggs of the queen - they have no fathers. Therefore, we were able to construct a linkage map by looking at rates of recombination between polymorphic DNA markers scattered randomly throughout the genome of the queen by looking directly at recombinational events in her gametes, the drone genomes. The drones used for con- structing the linkage map were also fathers of colonies. Using instrumental insemi- nation, we mated drones derived from the hybrid queen to high-pollen-hoarding strain queens that were sisters. As a consequence, most genetic variation observed between colonies was a consequence of genetic differences between the father drones, rather than the mother queens, so we assigned values of the colony phenotypes - the amount of pollen stored in the comb -to the fathers.

We constructed a linkage map with 365 DNA markers mapped to 26 linkage groups covering more than 3100 centiMorgans (CM, a measure of the frequency of genetic recombination between markers). Analyses [16] revealed two genomic regions with strong effects on the colony phenotype, des- ignated plnl and pZn2 (Figure 5). In combi- nation, these two regions explained 59% of the total phenotypic variance observed in our backcross population of colonies. Each had approximately the same effect. To vali- date independently these putative quantita- tive trait loci (QTLs) we produced an Fl hybrid queen and mated her to a single drone from the high-pollen-hoarding strain. The queen was heterozygous for two markers, each marker allele linked to a different putative QTL allele. We knew which marker alleles were inherited from each strain because we determined the genotypes of the parents of the hybrid queen. Because males are haploid, all worker progeny of this queen inherited the same high-strain allele at each marker locus, and the same QTL allele. Therefore, any genotypic differences among workers at the QTLs and marker loci were a consequence of genetic recombination in the hybrid queen. Returning forager progeny were randomly collected at the colony entrance, determined to be nectar or pollen collectors (some pollen collectors also collect nectar), then analysed to determine which marker alleles they had at each marker locus linked to each QTL.

Results of individual foraging behaviour confirmed those for the colony-level phenotype. Both regions significantly affected the probability that an individual would collect pollen or nectar, demonstrating their effect on foraging decisions. In addition, nectar foragers that inherited the high-strain allele at the marker near pZn2 collected significantly more dilute nectar than those that inherited the low-strain allele, thus suggesting that pln2 may be responsible for the observed differences $r response thresholds

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Figure 5 Major linkage groups containing mapped QTLs p/n7 (a) and p/n2 (b). The numbers to the left of the diagrammatic chromosomes represent the distances in centiMorgans between random amplified polymorphic DNA (RAPD) makers shown at the right. The most likely locations of the QTLs are indicated by the arrows. The line tracing to the right represents the logarithm of the likelihood odds ratio (LOD) that a QTL exists at each location along the linkage group. (Reproduced, with permission from [15].)

shown in the proboscis extension response tests.

Selected sociogenic pathways Colony-level selection resulted in allelic substitution at loci in two genomic regions. These loci have major effects on the decisions of foragers to collect pollen or nectar. One of these regions, pln2, also appears to affect the response thresholds of workers to sugar solutions, affecting their likelihood to forage for water and lower concentrations of nectar. Changes in individual foraging behaviour resulting from allelic substitutions changed the allocation of colonies with respect to the ratios of pollen and nectar foragers and resulted in changes in quantities of stored pollen. This represents a selectable sociogenic pathway from genes through processes of individual and colony- level development to the colony phenotype (Figure 6).

These two genomic regions, plnl and pln2, may also affect other pathways. For example, not only do co-fostered foragers from the high- and low-pollen-hoarding strain forage for pollen, nectar and water with different probabilities, they also differ in their rates of foraging for pollen and nectar, the sizes of the loads they collect, and the probability and vigour with which they recruit new foragers to pollen resources (G. Deng, K.D. Waddington and R.E. Page, unpublished data). We do not know to what extent these additional traits are determined by our mapped QTLs.

Conclusion Darwin believed that the evolution of workers and complex social behaviour was understandable with his theory of natural selection. The traditional approach to under- standing has been with comparative studies of social phenomena. Often underlying these studies is the assumption that observed phenotypic variation in colony organizational patterns is a consequence of variation in environments. With that model we need only understand the relationships between environments and organizational phenomena to understand why particular patterns exist. However, in order to truly understand the evolution of insect societies we need a model that incorporates the effects of genotype, environment, individual and colony-level developmental processes, and their interactions. At least for honey bees, the merger of behavioural and evolutionary ecology with behavioural and molecular genetics is stimulating the devel-

Genome Individual level

opment of a more complete model of social evolution, one where we cannot ask only ‘why’ we see particular patterns of social organization, but must ask also ‘how’ they evolved.

Acknowledgements This article was written while on sabbatical leave in the Institute for Ecology and Biology at the Technical University of Berlin with the support of an Alexander von Humboldt Senior Scientist Award. This work was originally presented as a Plenary Lecture at the Vth International Congress of Evolutionary and Systematic Biology held in Budapest, Hungary, 17-24 August 1996. The research presented was funded by grants from the National Science Foundation and the National Institute of Mental Health. 1 thank Joachim Erber and Robin Moritz for many stimulating hours of discussion and comments on earlier drafts.

Colony level Colony phenotype

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Figure 6 Sociogenic pathways that were altered by selection for the single colony-level phenotype, ‘the amount of pollen stored in the comb’. Components shown in bold italics represent pathways for which direct effects have been demonstrated from p/n7 and/or p/n2 through the different organizational levels and developmental processes to the colony phenotype.


References [l] Darwin, C.R. The Origin of Species.

MacMillan Publishing Co., New York, 1962.

[2] Bourke, A.F.G. and Franks, N. Social Evolution in Ants. Princeton University Press, Princeton, 1995.

[3] Robinson, G.E. and Page, R.E. Anim. Behav. 49,867-76, 1995.

[4] Sakagami, S.F. and Maeta, Y. In Animal Societies: Theories and Facts (eds Y. Ito, J.L. Brown and J. Kikkawa), pp. 1-16. Japan Scientific Society Press, Tokyo, 1987.

[5] Calderone, N.W. and Page, R.E. Behav.

Ecol. Sociobiol. 30, 219-26, 1992. [6] Seeley, T.D. Honeybee Ecology: A Study of

Adaptation in Social Life. Princeton University Press, Princeton, 1985.

[7] Winston, M.L. The Biology of the Honey Bee. Harvard University Press, Cambridge, MA, 1987.

[S] Fewell, J.F. and Winston, M.L. Behav. Ecol. Sociobiol. 30, 387-93, 1992.

[9] Fewell, J.F. and Page, R.E. Experientiu 49, 1106-12,1993.

[lo] Page, R.E. and Mitchell, S.D. In PSA I990 Vol. 2 (eds A. Fine, M. Forbes and L. Wessels), pp. 289-98. Philosophy of Science Association, East Lansing, MI,

1991. [ll] Page, R.E. and Robinson, G.E. Adv. Insecf

Phvsiol. 23. 117-69. 1991. [12] Page, R.E. &d For&k, M.K. Behav. Ecol.

Sociobiol. 36, 135-44, 1995. [13] Page, R.E., Waddington, K.D., Hunt, G.J.

and Fondrk, M.K. Anim. Behav. 50, 1617-25,199s.

[14] Hunt, G.J. and Page, R.E. Genetics 139, 1371-82, 1995.

[15] Hunt, G.J., Page, R.E., Fondrk, M.K. and Dullum, C.J. Genetics 141, 1.537-45, 1995.

[16] Lander, E.S. and Botstein, D. Genetics 121, 185-99, 1989.


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The evolution of insect societies