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Proc Biol Sci. Jan 7, 2006; 273(1582): 19–26.
Published online Oct 18, 2005. doi:  10.1098/rspb.2005.3291
PMCID: PMC1560005

Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp, Polistes canadensis

Abstract

Understanding how a single genome can produce a variety of different phenotypes is of fundamental importance in evolutionary and developmental biology. One of the most striking examples of phenotypic plasticity is the female caste system found in eusocial insects, where variation in reproductive (queens) and non-reproductive (workers) phenotypes results in a broad spectrum of caste types, ranging from behavioural through to morphological castes. Recent advances in genomic techniques allow novel comparisons on the nature of caste phenotypes to be made at the level of the genes in organisms for which there is little genome information, facilitating new approaches in studying social evolution and behaviour. Using the paper wasp Polistes canadensis as a model system, we investigated for the first time how behavioural castes in primitively eusocial insect societies are associated with differential expression of shared genes. We found that queens and newly emerged females express gene expression patterns that are distinct from each other whilst workers generally expressed intermediate patterns, as predicted by Polistes biology. We compared caste-associated genes in P. canadensis with those expressed in adult queens and workers of more advanced eusocial societies, which represent four independent origins of eusociality. Nine genes were conserved across the four taxa, although their patterns of expression and putative functions varied. Thus, we identify several genes that are putatively of evolutionary importance in the molecular biology that underlies a number of caste systems of independent evolutionary origin.

Keywords: paper wasp, social insect, caste determination, suppression subtractive hybridization

1. Introduction

An individual's phenotype is defined by its morphological, physiological and behavioural characteristics. Plasticity in these traits enables individuals to maximize their fitness in a variable environment, and thus plays an important role in adaptation, speciation and evolution (West-Eberhard 2002). Phenotypic adaptation is implemented at the level of the genes in response to fluctuating biotic and abiotic cues (Evans & Wheeler 2001; West-Eberhard 2002; Hofmann 2003). The environment of a social animal is particularly variable because of the additional influences of interactions with other group members. It is not surprising therefore that the eusocial insects (bees, wasps, ants and termites) exhibit some of the most extreme examples of phenotypic plasticity in the form of their female castes (West-Eberhard 1989; Hölldobler & Wilson 1990).

The eusocial insects exhibit a vast array of social complexity, encompassing varying degrees of caste differentiation. The most complex societies (e.g. honeybees and most ants) have morphologically distinct queen and worker castes that are determined pre-imaginally, and have sterile workers (cannot mate and produce diploid eggs). Castes in more simple societies (primitively eusocial insects, e.g. hover wasps and allodapine bees) are temporary, determined during adulthood and differ only in behaviour. Behavioural queen/worker castes are likely to represent the ancestral state of morphological castes, and thus provide insights into the evolution and origin of queen/worker castes that may not be obtained from studying advanced societies, where castes are more derived. As sociality has evolved multiple times in the social Hymenoptera (Wilson 1971), a key question is whether the genes associated with different caste systems are conserved across taxa and across different levels and origins of social complexity (Robinson 2002; Robinson & Ben-Shahar 2002). Differential gene expression amongst queen/worker castes has been studied previously in two species of advanced eusocial insects (the honeybee (Apis mellifera) and bumble-bee (Bombus terrestris) Corona et al. 1999; Evans & Wheeler 1999; Hepperle & Hartfelder 2001; Pereboom et al. 2005). Related studies have looked at the gene expression associated with worker behaviour in honeybee adults (Ben-Shahar et al. 2002; Kucharski & Maleszka 2002; Robinson 2002; Whitfield et al. 2003), wing polymorphism in ant queens and workers (Abouheif & Wray 2002; Tian et al. 2004), and soldier and worker caste differentiation in termites (Miura et al. 1999; Miura et al. 2003; Scharf et al. 2003). However, to date, there have been no studies on the relationship between genes and queen/worker castes in primitively eusocial insect societies.

Polistes paper wasps are primitively eusocial, exhibiting highly plastic behavioural phenotypes that are morphologically similar and determined during adulthood (Reeve 1991). Polistes females may vary in size, but on emergence all adults are capable of mating and laying haploid (male) and diploid (female) eggs. Although a female can remain as a worker all her life, she may become a queen if the existing queen dies or is over thrown, or if she founds a new colony (West-Eberhard 1969; Hughes et al. 1987; Peters et al. 1995). Nest-mates compete to realise their reproductive potential, forming a hierarchy of social dominance. The lowest ranked females are newly emerged from their pupal cells. Workers are intermediately ranked; they forage and care for brood. Queens are the highest ranked, and lay eggs (West-Eberhard 1986; Giray et al. 2005). The social hierarchy is maintained by physical aggression from higher ranked nestmates (Hughes et al. 1987) or by age/order of arrival at the nest (Hughes & Strassman 1988). Caste membership therefore changes gradually during a female's lifetime. Delaying caste determination until adulthood and maintaining high caste plasticity throughout life enables individuals to exploit their highly dynamic social environment (Jeanne 1972).

We present the first data on the molecular basis of behavioural queen/worker caste polyphenisms in a primitively eusocial society. Polistes canadensis is an ideal species in which to study castes because it is restricted to the relatively aseasonal tropics where, in contrast to temperate species of Polistes, both workers and queens are long-lived (Pickering 1980), caste is not influenced by the time of year that a female emerges (Mead & Gabouriaut 1993), and size/nutrition is unlikely to influence caste as queens do not hibernate (Strassmann et al. 1984; Sullivan & Strassmann 1984). We first identified genes that were differentially expressed between pairs of the three behavioural castes within P. canadensis (young females, Y; workers, W; and queens, Q). Next, we tested the hypothesis that the developmental gradient of young females to workers and workers to queens involves the gradual change in regulation of the same set of genes by comparing expression patterns of those genes identified as differentially expressed between one caste pair in other caste pairs. Lastly, we tested the hypothesis that the genes underlying behavioural castes (found in Polistes) are conserved in adults of advanced eusocial taxa (e.g. Apis and Bombus).

2. Material and methods

(a) Sample collection

In March 2002, P. canadensis colony members from 12 nests in Panama's Canal Zone were individually marked. Nests were post-emergence (i.e. had already produced adult offspring) with nine females ± 0.24 (s.e.). Censuses of nestmates were taken twice a day, every 3–5 days for one month, and behaviour recorded during 1 h observation periods on most census days. Queens were behaviourally dominant and the only egg-layer on their nests, and workers were low ranked females who foraged (West-Eberhard 1986). There was no queen turnover during the monitoring period. After one month queens and workers were removed directly from their nests using forceps and stored immediately either in liquid nitrogen (N2) or RNAlater reagent (Ambion), and subsequently at −80 °C (for N2 samples) or −20 °C (for RNAlater samples). Young females were preserved in the same way within 12 h of emergence on collected nest combs.

(b) Finding differentially expressed genes

(i) Construction of enriched libraries

Suppression subtractive hybridization (SSH) was used to identify differentially expressed genes (Diatchenko et al. 1996). Total RNA was extracted from five individuals of each phenotype (Trizol, Invitrogen) and purified into Messenger RNA (mRNA) (Nucleotrap kit, BD Clontech). Complementary DNA (cDNA) was synthesized from 2 μg mRNA, pooled from all five individuals per caste. Forward and reverse subtractions for each caste pair were performed following the PCR-Select cDNA subtraction protocol (BD Clontech). PCR-amplified products were cloned using pCR2.1 vector and grown in microtitre plates under standard conditions (Invitrogen).

(ii) Differential screening and selection of candidate genes

Differential screening eliminates false positives (Jin et al. 1997). Duplicate macroarrays, consisting of 960 clones per paired library, were constructed on nylon membranes using standard techniques (Hybond NX, Amersham). Subtracted cDNA probes derived from the SSH, were radio labelled (alpha-P32 dATPs) and hybridized to the macroarray membranes at 65 °C in Church buffer overnight (Sambrook & Russell 2001). Membranes were subsequently washed in SSC/SDS solution following the manufacturer's instructions (Amersham), and exposed to X-ray film (Kodak BioMax MS) for 3–72 h. Each macroarray was stripped and hybridized in turn with both members of its library's paired subtraction. Clones were chosen for sequencing if the product that hybridized with the opposite caste was at least twofold weaker than the hybridization product resulting with their own sample. Homologous matches with sequences in online databases (GenBank, Swiss-Prot, EMBL) were identified using Blast-x and Blast-n algorithms.

(iii) Quantification of differential expression

Total RNA was extracted from a further 10 individuals of each phenotype. Northern blots containing 15 μg total RNA from pooled samples (five individuals per phenotype) were constructed. RNA was quantified prior to loading using a spectrophotometer, and again after running the gel by recording the fluorescence of the mRNA smear for each sample using a CCD camera and Syngene GeneGenius software. Probes were prepared from the chosen clones by PCR amplification and isolation of the amplified band (QIA-quick gel extraction kit, Qiagen), and then radio labelled and hybridized to blots overnight at 65 °C. Blots were washed and exposed to X-ray film as described above. Peak heights were quantified from computer images of the scanned autoradiographs, corrected for the amount of RNA loaded on the gel (see above), and reported as ratios normalized across the three phenotypes to the phenotype showing strongest expression.

3. Results

Clones were chosen at random from those showing the strongest differential expression and 173 were successfully sequenced. Nine genes were present in more than one clone, with a maximum of eight clones containing the same sequence. Homologues with sequences on web-based databases were obtained for 105 sequences. Forty-three sequences were chosen for northern blot analysis (see table 1). Choice of sequences was based on three criteria: (i) all sequences showing significant homology to genes known to be differentially expressed in castes of other social Hymenoptera (n=9); (ii) a set of sequences showing significant homology to genes not known to be associated with caste (n=30); (iii) a set of sequences with no known homologues (n=4). Thirty-nine genes gave a detectable signal and over half of these were detected in all three phenotypes to varying degrees. Seven genes were equally expressed across all phenotypes (genes 33–39; i.e. have less than twofold differences in expression). Seven were detected in only one of the phenotypes: four were detected only in queens (genes 1–4), three in young females (genes 17–19), but none were detected only in workers. Nine genes were subjected to northern blot analysis for all three phenotypes on replicate blots containing independently isolated mRNAs (see table 1). All replicates gave highly comparable results (paired t-test t(0.05(2)27) p=0.102).

Table 1
Normalized relative expression levels for 43 genes screened in young females, workers and queens of Polistes canadensis, ranging from 0 (no expression detected), through intermediate values that indicate expression level as a proportion of the caste with ...

To determine how distinct the patterns of differential gene expression were between different phenotypes we analysed the correlation of expression levels between pairs of phenotypes of each of the 39 genes using Kendall partial rank–order correlations, which eliminates the possibility that a correlation is due to the association between any two phenotypes with the third (Seigel & Castellan 1988). The overall expression levels of genes in queens and young females were not significantly correlated (τ=−0.18, p>0.1; figure 1a), indicating that these two phenotypes differ substantially in gene expression patterns. In contrast, there were significant correlations in gene expression between queens and workers (τ=0.31, p<0.005; figure 1b) and between workers and young females (τ=0.38, p<0.001; figure 1c), indicating that workers do not differ substantially from queens and young females in gene expression.

Figure 1
Scatter plots and regression lines (solid) for raw expression levels (corrected for amount loaded on the gel) of genes between the different caste pairs. The dashed line shows equal expression between the two phenotypes. The dotted lines show the upper ...

We further assessed how gene expression patterns changed with the phenotypic transitions that commonly occur in a P. canadensis colony by looking for trends in the direction of gene expression between young females, workers and queens. The majority of the genes (81% (26/32)) were either up- or down-regulated (more than twofold expression difference) with increasing social status (figure 2a (n=16), b (n=10), respectively), indicating that workers generally express caste-associated genes at levels that are intermediate between those of young females and queens. Only six genes deviated from this pattern, either being not detected (figure 2c, n=4) or up-regulated in workers (figure 2d, n=2). Some of the expression differences might be explained in terms of the genes' functional groups (table 2). All of the genes associated with metabolism in our sample had expression levels that were twofold (or more) higher in queens than in young females (n=7 genes, Fisher's exact p=0.00058), indicating that queens over express metabolic genes relative to young females.

Figure 2
Normalized expression of differentially expressed genes in young females (Y), workers (W) and queens (Q). Patterns are determined using greater than or equal to twofold difference in expression between castes. Zero indicates no detectable expression, ...
Table 2
Mean normalized gene expression (mean±s.e.) for each caste within main functional groups.

We investigated whether any of the genes we have identified in our study were also differentially expressed in adult castes of eusocial insects in more complex (socially advanced) societies where queen and worker castes differ in morphology. We excluded larval gene expression studies because gene functions in larvae and adults stages are not comparable (Pereboom et al. 2005). Gene expression data for adult castes were available for three species: two bees (A. mellifera and B. terrestris) and one ant (the fire ant, Solenopsis invicta). Eight of the genes we found in P. canadensis were differentially expressed between castes of one or more of these species (see table 3). Another gene, hexamerin 2, was expressed equally in alate and dealate queens of S. invicta. There were some consistent patterns of expression for particular genes by queens and workers of the different species. Worker specific genes included those associated with heat shock and imaginal disk development, which were up-regulated in foraging workers for both P. canadensis and A. mellifera, and peroxiredoxin which was worker expressed in both P. canadensis and B. terrestris. Cytochrome oxidase was associated with the absence of reproduction in B. terrestris workers, but up-regulated in both queens and workers of P. canadensis. Three genes associated with mature (dealate) queens in S. invicta were up-regulated by P. canadensis queens (vitellogenin, major royal jelly protein (MRJP) and hexamerin 2). Transferrin was up-regulated in virgin queens and foragers of A. mellifera but up-regulated by only queens in P. canadensis.

Table 3
Comparison of genes expressed by behavioural castes in P. canadensis with genes associated with morphological castes amongst adults of more complex eusocial insects. (In each case the phenotype with the highest expression level is indicated. ‘Not ...

4. Discussion

We have isolated 32 genes whose differential expression is associated with young female, worker and queen phenotypes in adult females of the paper wasp, P. canadensis. The social biology of a Polistes colony is governed by the ontogenetic transitions from young adult female to queen (see §1). Our first hypothesis was that the gene expression patterns associated with the three behavioural phenotypes would reflect these important biological changes. Our data support this. First, overall gene expression levels in workers correlated significantly with both queens and young females, whilst there was no significant correlation in gene expression levels between queens and young females (figure 1). Second, 81% of the caste-associated genes were either up- or down-regulated along the social gradient, such that workers usually express genes at levels that are intermediate between those of young females and queens (figure 2). Thirdly, only two genes were up-regulated in workers (figure 2d). These findings demonstrate that the worker expression patterns are intermediate to those of queens and young females, reflecting the flexible, temporary nature of the behavioural castes in Polistes. The workers used in our study had specialized in foraging. It remains to be seen whether individual P. canadensis workers who show a tendency to forage, nest guard or nurse brood show greater differentiation at the transcriptome level than is apparent from our study (Giray et al. 2005).

Young, newly emerged females in simple societies are likely to be analogous to the totipotent, early instar larvae in more complex societies, which have yet to embark on a queen or worker developmental pathway. The gene expression patterns of young females were more similar to workers than queens. This is consistent with the biology of P. canadensis, since in nature young females invariably become workers after emergence, rather than queens (Pickering 1980). However, there were some genes that were specifically up-regulated by young females, and these may be associated with either totipotency or the final stages of maturation. These genes include homologues of transposable elements, which are thought to be involved in mutagenesis in Drosophila (Kaminker et al. 2002).

Genes that putatively code for metabolic enzymes were up-regulated in queens, which is consistent with egg production being metabolically costly. Queens expressed nine genes that were not detected in workers, and up-regulated a further six genes relative to workers (table 1). Not all these genes are obviously associated with reproduction, suggesting that there is more to being a queen than simply producing eggs. For example, transferrin is up-regulated eightfold in queens relative to workers and has anti oxidant and antibacterial functions (Kucharski & Maleszka 2003). Caste determination mechanisms in the eusocial Hymenoptera are closely linked with changes in levels of ecdysteroids and juvenile hormone (JH) (Bloch et al. 2002). We found no genes that were obviously associated with production of these hormones in our study, although the uptake of vitellogenin is stimulated by the presence of JH (Bloch et al. 2002), and was up-regulated in P. canadensis queens.

Our second hypothesis was that genes associated with queen and worker behaviours in adult P. canadensis wasps would also be differentially expressed in other eusocial taxa. There is currently little gene expression data available for adult eusocial insects. We found data on two bees (A. mellifera and B. terrestris) and one ant (S. invicta) to compare with P. canadensis, although the latter examined only dealate and alate queens. Heat shock proteins are associated with stress, particularly exposure to high temperatures, as well as being molecular chaperones. These were up-regulated in foragers of A. mellifera relative to nursing workers (Whitfield et al. 2003), and in foragers of P. canadensis relative to queens, highlighting the potential importance of this family of genes in foraging behaviour. Vitellogenin was up-regulated in mature queens of P. canadensis and S. invicta, but in A. mellifera it was expressed by both queens and nurse (hive) workers. In A. mellifera vitellogenin is involved with brood-food production (jelly) (Amdam et al. 2003). Vitellogenin in Polistes, and probably in other primitively eusocial species, has not evolved such a complex role and is instead a queen-associated gene involved mainly in egg production (Giray et al. 2005). MRJP is involved in secretion of royal jelly in A. mellifera workers (Whitfield et al. 2003). In P. candensis, it was not detected in foragers but was up-regulated strongly in queens. This is comparable with S. invicta where MRJP-like genes are up-regulated in dealate queens, suggesting that they are associated with mature queen behaviour (Tian et al. 2004). Both MRJP and vitellogenin appear to be caste-associated genes in adults across taxa, but their functions in Apis have apparently diverged.

Polistes, Solenopsis, Apis and Bombus represent four independent origins of eusociality (Carpenter 1991; Cameron & Mardulyn 2001). Given the relatively small number of genes examined in any of these studies (with the exception of those on Apis) it was surprising to find 9 of the 32 genes identified in this study were also differentially expressed during caste determination across 2–4 of these taxa. These genes are putatively of evolutionary importance in queen and worker behaviours, since they have arisen independently in several eusocial taxa through either conservation or convergence. However, few genes have been examined in more than two species, there is limited evidence for consistency in the direction of caste-associated expression across taxa, and specific gene functions in the different taxa remain undetermined.

Our study provides the first base line data for sociogenomic studies on the proximate mechanisms underlying behavioural phenotypes in primitively eusocial insects. Within-family comparative studies of species sharing a common evolutionary ancestor, but showing a range of social complexity, promise to further our understanding of the molecular basis of caste evolution and phenotypic plasticity.

Acknowledgments

We thank M. Dijkstra and N. J. B. Isaac for assistance in the field, A. F. G. Bourke and M. J. West-Eberhard for comments, and W. T. Wcislo for logistical support. S.S. was supported by a Postdoctoral Fellowship and the research was funded by a Scholarly Studies Grant, both awarded by the Smithsonian Institute.

References

  • Abouheif E, Wray G.A. Evolution of the gene network underlying wing polyphenism in ants. Science. 2002;297:249–252. 10.1126/science.1071468 [PubMed]
  • Amdam G.V, Norberg K, Hagen A, Omholt S.W. Social exploitation of vitellogenin. Proc. Natl Acad. Sci. USA. 2003;100:1799–1802. 10.1073/pnas.0333979100 [PMC free article] [PubMed]
  • Ben-Shahar Y, Robichon A, Sokolowski M.B, Robinson G.E. Influence of gene action across different time scales on behaviour. Science. 2002;296:741–744. 10.1126/science.1069911 [PubMed]
  • Bloch G, Wheeler D.E, Robinson G.E. Endocrine influences on the organisation of insect societies. In: Pfaff D, Arnold A, Etgen A, Fahrbach S, Moss R, Rubin R, editors. Hormones, brain behaviour. vol. 3. Academic; New York: 2002. pp. 195–235.
  • Cameron S.A, Mardulyn P. Multiple molecular data sets suggest independent origins of highly eusocial behaviour in bees (Hymenoptera: Apinae) Syst. Biol. 2001;50:194–214. 10.1080/10635150151125851 [PubMed]
  • Carpenter J.M. Phylogenetic relationships and the origin of social behaviour in the Vespidae. In: Ross K.C, Matthews R.W, editors. The social biology of wasps. Cornell University Press; Ithaca, NY: 1991. pp. 7–32.
  • Corona M, Estrada E, Zurita M. Differential expression of mitochondrial genes between queens and workers during caste determination in the honeybee, Apis mellifera. J. Exp. Biol. 1999;202:929–938. [PubMed]
  • Diatchenko L, et al. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl Acad. Sci. USA. 1996;93:6025–6030. 10.1073/pnas.93.12.6025 [PMC free article] [PubMed]
  • Evans J.D, Wheeler D.E. Differential gene expression between developing queens and workers in the honey bee, Apis mellifera. Proc. Natl Acad. Sci. USA. 1999;96:5575–5580. 10.1073/pnas.96.10.5575 [PMC free article] [PubMed]
  • Evans J.D, Wheeler D.E. Gene expression and the evolution of insect polyphenisms. BioEssays. 2001;23:62–68. 10.1002/1521-1878(200101)23:1%3C62::AID-BIES1008%3E3.0.CO;2-7 [PubMed]
  • Giray T, Giovanetti M, West-Eberhard M.J. Juvenile hormone, reproduction, and worker behaviour in the neotropical social wasp Polistes canadensis. Proc. Natl Acad. Sci. USA. 2005;102:3330–3335. 10.1073/pnas.0409560102 [PMC free article] [PubMed]
  • Hepperle C, Hartfelder K. Differentially expressed regulatory genes in honey bee caste development. Naturwissenschaften. 2001;88:113–116. 10.1007/s001140000196 [PubMed]
  • Hofmann H. Functional genomics of neural and behavioural plasticity. J Neurobiol. 2003;54:272–282. 10.1002/neu.10172 [PubMed]
  • Hölldobler B, Wilson E.O. Springer; Berlin: 1990. The ants.
  • Hughes C.R, Strassman J.E. Age is more important than size in determining dominance among workers in the primitively eusocial wasp, Polistes instabilis. Behaviour. 1988;107:1–15.
  • Hughes C.R, Beck M.O, Strassmann J.E. Queen succession in the social wasp, Polistes annularis. Ethology. 1987;76:124–132.
  • Jeanne R.L. Social biology of the Neotropical wasp, Mischocyttarus drewseni. Bull. Mus. Comp. Zool. Harv. Univ. 1972;144:63–150.
  • Jin H, Cheng X, Diatchenko L, Siebert P.D, C H. Differential screening of a subtracted cDNA library: a method to search for genes preferentially expressed in multiple tissues. BioTech. 1997;23:1084–1087. [PubMed]
  • Kaminker J.S, Bergman C.M, Kronmiller B, Carlson J, Svirskas R, Patel S, Frise E, Wheeler D.A, Lewis S.E, Rubin G.M, Ashburner M, Celniker S.E. The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol. 2002;3:0084.1–0084.20. (See http://www.fruitfly.org/about/pubs/genome_biology/gb-2002-3-12-research0084.pdf) [PMC free article] [PubMed]
  • Kucharski R, Maleszka R. Evaluation of differential gene expression during behavioural development in the honeybee using microarrays and northern blots. Genome Biol. 2002;3 10.1186/gb-2002-3-2-research0007 [PMC free article] [PubMed]
  • Kucharski R, Maleszka R. Transcriptional profiling reveals mutilfunctional roles for transferrin in the honeybee, Apis mellifera. J. Insect Sci. 2003;3:1–8. [PMC free article] [PubMed]
  • Mead F, Gabouriaut D. Post-eclosion sensitivity to social context in Polistes dominulus Christ females (Hymenoptera: Vespidae) Insect. Soc. 1993;40:11–20. 10.1007/BF01338829
  • Miura T, Kamikouchi A, Takeuchi H, Natori S, Kubo T, Matsumoto T. Soldier caste-specific gene expression in the mandibular glands of Hodotermopsis japonica (Isoptera: Termopsidae) Proc. Natl Acad. Sci. USA. 1999;96:13 874–13 879. 10.1073/pnas.96.24.13874 [PMC free article] [PubMed]
  • Miura T, Koshikawa S, Matsumoto T. Winged presoldiers induced by a juvenile hormone analog in Zootermopsis nevadensis: implications for plasticity and evolution of caste differentiation in termites. J. Morphol. 2003;257:22–32. 10.1002/jmor.10100 [PubMed]
  • Pereboom J.J.M, Jordan W.C, Sumner S, Hammond R.L, Bourke A.F.G. Differential gene expression in queen–worker caste determination in bumblebees. Proc. R. Soc. B. 2005;272:1145–1152. 10.1098/rspb.2005.3060 [PMC free article] [PubMed]
  • Peters J.M, Queller D.C, Strassmann J.E, Solis C.R. Maternity assignment and queen replacement in a social wasp. Proc. R. Soc. B. 1995;260:7–12. [PubMed]
  • Pickering, J. 1980 Sex ratio, social behaviour and ecology in Polistes, Pachysomoides and Plasmodium Ph.D. thesis, Harvard University, Cambridge, Massachusetts.
  • Reeve H. In: Social biology of wasps. Ross K.G, Matthews R.W, editors. Cornell University Press; Ithaca, NY: 1991. pp. 99–148.
  • Robinson G.E. Genomics and intergrative analysis of division of labour in honeybee colonies. Am. Nat. 2002;160(Suppl.):S160–S172. 10.1086/342901 [PubMed]
  • Robinson G.E, Ben-Shahar Y. Social behaviour and comparative genomics: new genes or new gene regulation? Genes Brain Behav. 2002;1:197–203. 10.1034/j.1601-183X.2002.10401.x [PubMed]
  • Sambrook J, Russell D.W. 3rd edn. Cold Spring Harbour Laboratory Press; New York: 2001. Molecular cloning: a laboratory manual.
  • Scharf M.E, Wu-Scharf D, Pittendrigh B.R, Bennett G.W. Caste- and development-associated gene expression in a lower termite. Genome Biol. 2003;R62:1–11. [PMC free article] [PubMed]
  • Seigel S, Castellan N.J. McGraw-Hill; New York: 1988. Non-parametric statistics for the behavioural sciences.
  • Strassmann J.E, Lee R.E, Jr, Rojas R.R, Baust J.G. Caste and sex differences in cold-hardiness in the social wasps, Polistes annularis and P. exclamans (Hymenoptera: Vespidae) Insect. Soc. 1984;31:291–301.
  • Sullivan J.D, Strassmann J.E. Physical variability among nest foundresses in the polygynous social wasp, Polistes annularis. Behav. Ecol. Sociobiol. 1984;15:249–256. 10.1007/BF00292986
  • Tian H, Vinson B, Coates C.J. Differential gene expression between alate and dealate queens in the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae) Insect Biochem. Mol. Biol. 2004;34:937–949. 10.1016/j.ibmb.2004.06.004 [PubMed]
  • West-Eberhard M.J. The social biology of polistine wasps. Misc. Publ. Mus. Zool. Univ. Mich. 1969;140:1–101.
  • West-Eberhard M.J. Dominance relations in Polistes canadensis (L.), a tropical social wasp. Monit. Zool. Ital. (NS) 1986;20:263–281.
  • West-Eberhard M.J. Phenotypic plasticity and the origins of diversity. Ann. Rev. Ecol. Syst. 1989;20:249–278. 10.1146/annurev.es.20.110189.001341
  • West-Eberhard M.J. Oxford University Press; New York: 2002. Developmental plasticity and evolution.
  • Whitfield C.W, Cziko A.M, Robinson G.E. Gene expression profiles in the brain predict behaviour in individual honey bees. Science. 2003;302:296–299. 10.1126/science.1086807 [PubMed]
  • Wilson E.O. Harvard University Press; Cambridge, MA: 1971. The insect societies.

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