What can mechanisms underlying derived traits tell us about the evolution of social behavior? Treanore E, Derstine N, Amsalem E. Accepted to the Annals of the Entomological Society of America (August 2020). A review paper emphasizing the importance of studying mechanistic, rather than functional continuity of traits by discussing how derived traits can provide useful insights on social evolution even if they are absent or rare in species with a lower social organization. We discuss two examples of derived traits, morphological differences in female castes, and primer pheromones regulating female reproduction, demonstrating how their underlying mechanisms can be used to understand major transitions in the evolution of social behavior.
Built to change: dominance strategy changes with life stage in a primitively eusocial bee. M Orlova, ED Treanore, E Amsalem. Accepted to Behavioral Ecology. The queens’ strategy to monopolize reproduction changes with life stage, shifting fromovert aggression tochemical signalling as the queen gets older. Particularly, old queens exhibited a higher ratio of short to long cuticular hydrocarbons compared to young queens, an endogenous shift that was attributed to age. in the figure: a model showing aggression and short to long CHC ratio in young and old queens, respectively, predict worker oocyte size
M Orlova, JA Starkey, E Amsalem. A small family business: synergistic and additive effects of the queen and the brood on worker reproduction in a primitively eusocial bee. 2020. Journal of Experimental Biology 223 (3). In this study we aim at disentangling the roles of the brood and the queen in regulating worker reproduction in primitively eusocial bees. We compared behavior, physiology and gene expression in the presence of queen, brood, both or none. We found that the queen and the brood coordinate synergistically, additively, and sometimes even redundantly to regulate worker behavior and reproduction. In the figure, workers egg laying is partially reduced in the presence of brood and fully inhibited in the presence of a queen, either with or without a brood. Ovary activation, on the other hand (lower figure) is not reduced in the presence of the brood, partially reduced in the presence of the queen (without brood) and fully inhibited in the presence of both queen and brood.
Treanore E, Kiner JM, Kerner ME, Amsalem E. Shift in worker physiology and gene expression pattern from reproductive to diapause-like with colony age in the bumble bee Bombus impatiens". 2020 Journal of Experimental Biology 223 (9). Bumble bee worker physiology and gene expression patterns shift from reproductive-like to diapause-like as the colony ages. Workers eclosing early in the colony cycle had increased egg-laying and ovarian activation, and reduced cold tolerance, body size, mass, and lipid content in the fat body, in line with a reproductive-like profile, while late-eclosing workers exhibited the opposite characteristics. Similar differences between early and late season workers were found in the expression patterns of several candidate genes associated with reproduction and diapause. In the figure: worker cold tolerance increases with colony age
Starkey J, Derstine N, Amsalem E. (2019) Do bumblebees produce brood pheromone? 45, pages725–734 (2019). Worker egg laying is reduced in the presence of young larvae. Is the effect mediated by pheromones? Here we showed that workers are behaviorally attracted to larvae (left figure), but the effect is not mediated by signals produced by the brood, either non-volatile or volatile (middle figure). In a separate set of experiments we showed that young larvae are more vulnerable to starvation and egg inhibition is higher in the presence of starved larvae (right figure)
Starkey J, Brown A, Amsalem E. (2019) The road to sociality: Brood regulation of worker reproduction in the simple eusocial bee Bombus impatiens. Animal Behaviour 154, 57-65. Young larvae reduced worker egg laying but not ovary size in B. impatiens. The effect is replicable regardless of worker age, relatedness to brood or brood parentage/sex. In the upper figure, the effect of eggs, larvae, pupae and wax control on egg laying behavior in random age workers. Same findings were found for workers that were introduced to brood as callows (lower figure).
Orlova M & Amsalem E. (2019) Context matters: plasticity in response to pheromones regulating reproduction and collective behavior in social Hymenoptera. Current Opinions in Insect Science 35:69-76. A review paper discussing the importance of context to the way pheromones mediating social behavior in Hymenoptera act. Speicifically we discuss the differences between reproductive and maintanance signaling.
Amsalem E, Galbraith D, Cnaani J, Teal P, Grozinger CM. (2015) Conservation and modification of genetic and physiological toolkits underpinning diapause in bumble bee queens. Molecular Ecology, 24(22):5596-5616 PDF. In this study we examined the physiological and transcriptomic changes associated with diapause and CO2 treatment, which causes B. terrestris queens to bypass diapause. We performed comparative analyses with genes previously identified to be associated with diapausein the Dipteran Sarcophaga crassipalpis and with caste differentiation in bumble bees. We found a substantial overlap between genes related to caste determination and diapause in bumble bees and demonstrate an intriguing interplay between pathways underpinning adaptation to environmental extremes and the evolution of sociality in insects.
Amsalem E, Orlova M, Grozinger CM (2015). A conserved class of queen pheromones? Reevaluating the evidence in bumble bees (Bombus impatiens). The Proceedings of the Royal Society London B, Vol 282(1817) PDF. A study conducted in response to several studies claiming hydrocarbons serve as a conserved class of queen pheromones in social insects. We repeated and extanded the experiment in bumble bees using Bombus impatiens, quantified and tested several different ubiquitious hydrocarbons in the cuticule of females, examine two types of workers (newly emerged and random-age workers taken from queenright colonies), and measured several variables related to reproduction: ovary activation (in the figure above), egg laying and oocyte regression. We found no evidence for reproductive inhibition of workers by cuticular hydrocarbons.
Amsalem E, Grozinger CM, Padilla M, Hefetz A (2015) The physiological and genomic bases of bumble bee social behavior. In Amro Zayed, Clement Kent, editors: Genomics, Physiology and Behavior of Social Insects, Vol 48, AIIP, UK: Academic Press, 2015, pp. 37-93 PDF. A review paper describing the current state of knowledge about the evolutionary,ecological, behavioural, physiological, chemical, and genomic mechanisms and factorsunderpinning bumble bee social behaviour throughout the colony cycle. Photo by Erin Treanore.
Amsalem E, Kiefer J, Schultz S, Hefetz, A (2014) The effect of caste and reproductive state on the chemistry of the cephalic labial glands secretion of Bombus terrestris. Journal of Chemical Ecology 48(8): 900-912 PDF. Chemical analysis of the labial gland secretion of Bombus terrestris females show a context-dependent composition with sterile females possessing large amounts of fatty acid dodecylesters, ranging from dodecyl hexanoate to dodecyl oleate,compared to small amounts in fertile females. Significant reduction in the dodecyl esters also was found in queens at the competition phase, where worker reproduction, aggression, and gyne differentiation occur. We proposed that the labial gland esters provide yet another signal of reproductive inactivity.
Amsalem E, Teal P, Grozinger CM, Hefetz A (2014) Precocene-I inhibits juvenile hormone biosynthesis, ovarian activation, aggression and alters sterility signal production in bumble bee (Bombus terrestris) workers. Journal of Experimental Biology. 217 (17): 3178-3185. Precocene-I, a JH inhibitor, applied to three-worker groups decreased JH titer and ovarian activation, irrespective of the bees’ dominance rank within the group, and was remedied by JH replacement therapy. Precocene-I also decreased aggressiveness and increased ester-sterility signal production; these changes were rank-dependent, and affected mainly the most reproductive and the least aggressive workers, respectively, and could not be remedied by JH replacement therapy.
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Show me your Dufour's gland and I'll tell you who you are: caste and physiology specific signals in Bombus impatiens. NT Derstine, G Villar, A Hefetz, J Millar, E Amsalem. bioRxiv. Compounds in the Dufour’s gland of Bombus impatiens females act as caste-and physiology-specific signals and are used by workers to discriminate between workers of different social and reproductive status. in the figure: Workers and queen groups are seperated by the Dufour's gland compounds, attributed mostly by esters and alkanes.
Evolution of olfactory functions on the fire ant social chromosome. Cohanim AB, Amsalem E, Saad R, Shoemaker D, Privman E. Genome biology and evolution 10 (11), 2947-2960. We identified acluster of 23 odorant receptors in the nonrecombining region of the social chromosome of the fire ant solenopsis invicta. We found evidence for positive selection on several tree branches and significant differences between the SB and Sb haplotypes of these genes. The most dramatic difference is the complete deletion of two genes in Sb (shown in the figures above), suggesting that the evolution of polygyne social organization involved adaptations in olfactory genes
Amsalem E, Hefetz A. (2018) Preface: Pheromone-mediation of female reproduction and reproductive dominance in social species. Journal of Chemical Ecology. A preface for a special issue on pheromones regulating reproduction in insects edited by Etya Amsalem and Abraham Hefetz.
Amsalem E, Grozinger CM. (2018) The importance of holistically evaluating data: a comment on Holman 2018. Behavioral Ecology. Invited commentary on Holman 2018 meta-analysis of queen pheromones in social insects. We emphasized that data collection and analysis were not done uniformly, potentially leading to biased conclusions.
Amsalem E, Padilla M, Schreiber P, Altman N, Hefetz A, Grozinger CM. (2017) Do bumble bee (Bombus impatiens) queens signal their reproductive and mating status to their workers? Journal of Chemical Ecology 43 (6): 563-572 PDF. Any egg laying queens, regardless of mating status can inhibit ovary activation in B. impatiens workers (left figure), but workers can differentiate between queens of different mating status as evidence by reduce vitellogenin expression levels in the presence of newly mated queen. cuticular wash of queens do not induce the same effect as live queens (right figure).
Amsalem E, Grozinger CM. (2017) Evaluating the molecular, physiological and behavioral impacts of CO2 narcosis in bumble bees (Bombus impatiens) Journal of Insect Physiology 101:57-65. Carbon dioxide (CO2) has pleiotropic effects on bumblebee queens, it induces transition to reproduction in 3 days and lipid depletion in 24 hours, increases aggression and flight behavior, improve immune function and lead to reduction in the expression of antioxidant enzyme transcripts
Padilla M, Amsalem E, Altman N, Hefetz A, Grozinger CM (2016) Chemical communication is not sufficient to explain reproductive inhibition in the bumblebee Bombus impatiens. Royal Society Open Science, in press PDF. Queen-initiated behavioural interactions is necessary to establish reproductive dominance over workers. Exposure to queen-produced volatiles, brood-produced volatiles and direct contact with pupae did not reduce worker ovary activation; only direct contact with the queen could reduce ovary activation. Caged queen marginally reduced worker aggression and expression of an aggression-associated gene relative to queenless workers.
Shpigler, H, Amsalem E, Huang ZY, Cohen M, Siegel AJ, Hefetz A, Bloch G (2014) Gonadotropic and physiological functions of juvenile hormone in bumblebee (Bombus terrestris) workers. PLoS ONE 9(6): e100650. In this study, we performed allatectomy and replacement therapies to manipulate JH levels in B. terrestris workers. Allatectomized worker bees showed remarkable reduction in ovarian development, egg laying, Vitellogenin and Krüppel homolog 1 fat body transcript levels, hemolymph Vitellogenin protein abundance, wax secretion, egg-cell construction and reduction in the amount of ester component in Dufour's gland secretion, which is thought to convey a social signal relating to worker fertility. .These effects were reverted, at least partially, by treating allatectomized bees with JH-III, the natural JH of bees.
Amsalem E, Malka O, Grozinger C, Hefetz A (2014) Exploring the role of juvenile hormone and vitellogenin in reproduction and social behavior in bumble bees. BMC Evolutionary Biology 14:45. In this study we characterized vitellogenin RNA expression levels (vg) in B. terrestris and showed that vg is not associated with task and only partially associated with worker age, queen presence, and caste (queen vs worker). Both vg and ovarian activation were significantly associated with levels of aggression experienced by workers (figure above) and treatment with juvenile hormone did not affect vg levels in queenless groups. Overall, social interactions saeem to affect vg levels more strongly than a worker’s reproductive physiological state, and juvenile hormone and vg are uncoupled in this species.
Amsalem E, Shpigler H, Bloch G, Hefetz A (2013) Dufour’s gland secretion, sterility and foraging behavior: Correlated behavior traits in bumblebee workers. Journal of Insect Physiology 59(12), 1250-1255. Here we show that ester production in the dufour gland of B. terrestris workers is not only correlated with sterility but also with foraging behavior, signaling cooperative behavior by subordinate workers. We demonstrate that foragers produce larger amounts of esters compared to non-foragers, and that their amounts positively correlate with foraging efforts.
Amsalem, E, Shamia, D and Hefetz, A (2013) Aggression or ovarian development as determinants of reproductive dominance in B. terrestris: interpretation using a simulation model. Insectes Sociaux 60 (2), 213-222. Here we used a combination of simulation model and data derived in the lab for B. terrestris queenless worker groups to answer how do workers established a dominance hierarchy. We demonstrated that previous encounter experience (win/lose) rather than mutual assessment of reproductive status determines and maintains hierarchy in B.terrestris.
Amsalem, E., Twele, R., Francke, W. And Hefetz, A (2009) Reproductive competition in the bumblebee B. terrestris: Do workers advertise sterility? Proceedings of the Royal Society of London B. 276 (1660): 1295-1304. The Dufour gland secretion of egg-laying queens is composed of a series of aliphatic hydrocarbons (alkanes and alkenes), while that of sterile workers contains in addition octyl esters, dominated by octyl hexadecanoate and octyl oleate. These esters disappear in workers with developed ovaries, whether queenright or queenless, rendering their secretion queen-like. This constitutes an unusual case in which the sterile caste, rather than the fertile one, possesses extra components.
Amsalem, E. and Hefetz, A (2011) The effect of group size on the interplay between dominance and reproduction in B. terrestris. PLoS One 6(3): e18238. We investigated the effect of group-size in B. terrestris queenless workers on two major reproduction-dominance correlates: between-worker aggression, and pheromone production. We found that in all groups aggression was not evenly distributed with the α-worker performing most of the aggressive acts. Moreover, aggression by the α-worker increased proportionally with group-size. However, while in small groups the α-worker monopolized reproduction, in larger groups several workers shared reproduction, We proposed that division of labor in workers is density-dependent.
Amsalem, E. and Hefetz, A (2010) The appeasement effect of sterility signaling in dominance contests among B. terrestris workers. Behavioral Ecology and Sociobiology. 64 (10): 1685-1694. Using pairs of B. terrestris workers, we show that workers establish dominance hierarchies using overt aggression within 3–4 days. Thereafter, the aggression drastically decreased, and dominance was maintained mostly by ritualized agonistic behavior. The behaviorally dominant bee lost the ester compounds that workers produce in their Dufour's gland (the so-called “sterility signal”) concomitantly with the development of her ovaries. The other bee announced as subordinate by continuously producing high amounts of those esters (correlation is demonstrated in the figure above). The findings suggest that sterility signaling serves as an appeasement signal to pacify the dominant bee.
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