The Evolution of Colonial Insects

Signals produced by queens in eusocial colonies, most commonly in the form of CHC pheromones, indicate the queens presence and/or fertility to workers who then abandon their own reproduction and help with rearing siblings (Nonacs, 1993). When a colony loses its queen or the queen loses fertility, the queen signal diminishes and non sterile workers will start to lay eggs themselves (Nonacs, 1993). Although in some smaller colonies queen signaling may be communicated through dominance behaviour  such as aggressive queen-worker interactions, and egg policing (Van Zweden et all, 2014) in all others it is achieved chemically. In very large colonies (>1000 individuals) the colony size even necessitate indirect communication about the queen's presence and fertility is further, with messenger workers who spread the queen pheromone throughout the colony (Naumann et al., 1991). Workers will even use queen signals to control each others reproduction, so called egg policing, where workers will destroy eggs laid by other workers (Ratnieks, 2008).
 

        Figure 1 -Evolutionary history of sterility-inducing queen signals.      .

There are two completing theories on how queen pheromones function: either as honest signals or as manipulative agents used to control the colony. According to the queen signal hypothesis, workers are voluntarily responding to the queen’s pheromones to the extent that it serves their own evolutionary interests (Ratneiks, 2008). This would imply that the workers inside the colony are always capable of egg laying but it is more evolutionary advantageous them to forego reproduction. 

On the other hand, the queen control hypothesis suggests that the queen’s pheromones chemically manipulate the workers to remain sterile, against the workers’ own reproductive interests. In this case, the workers are prevented from laying eggs, even if some would benefit from direct reproduction (Wenseleers and Ratneiks, 2006). This hypothesis suggests that the workers and queen may be locked in a evolutionary arms race, with workers struggling to reproduce while being involuntarily sterilised by the queens potent pheromones.

While the exact nature of the queen-worker relationship may be still be under dispute, the actual evolutionary origins of the CHC pheromones (Figure 1) that compose the queen signals are of less contention. There is significant evidence that the production of these queen CHCs are intrinsically linked to ovarian development and mating status (Monnin, 2006). The ovarian by-product hypothesis suggests they the queen's CHC cocktail has evolved from compounds that are produced in solitary insects to signal the onset of ovarian activity and successful mating to other potential mates (Caliari Oliviera et al, 2015).

References:
Caliari Oliveira, R., Oi, C.A., do Nascimento, M.M.C., Vollet-Neto, A., Alves, D.A., Campos, M.C., Nascimento, F., Wenseleers, T., 2015, The origin and evolution of queen and fertility signals in Corbiculate bees BMC Evol. Biol., 15, p. 254 
 
Naumann, K., Winston, M.L., Slessor, K.N. Prestwich, G.D, 1991, Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone ,Behav. Ecol. Sociobiol., 29, pp. 321-332 

Nonacs P., 1993. The role of queen pheromones in social insects: queen control or queen signal? Anim Behav45: 787–94.

Monnin, T., 2006, Chemical recognition of reproductive status in social insects, Ann. Zool. Fenn., 43, pp. 515-530 

Ratnieks FLW, Wenseleers T., 2008, Altruism in insect societies and beyond: voluntary or enforced?, Trends Ecol Evol23: 45–52.

Wenseleers T, Ratnieks FL., 2006, Enforced altruism in insect societies. Nature444: 50.

Van Zweden JS, Bonckaert W, Wenseleers T, d’Ettorre P., 2014, Queen signaling in social wasps. Evolution68: 976–86.

Figure:

Evolutionary history and identity of sterility-inducing queen and fertility signals in social insects, https://bio.kuleuven.be/ento/pdfs/Oi_et_al-2015-BioEssays.pdf, 9/5/2020