Local differences in parasitism and competition shape defensive investment in a polymorphic eusocial bee

Many colonial animals rely for their defense on a soldier caste. Adaptive colony demography theory predicts that colonies should flexibly adjust the investment in different worker castes depending on the colony needs. For example, colonies should invest more in defensive workers (e.g., soldiers) in dangerous environments. However, evidence for this prediction has been mixed. We combined descriptive and experimental approaches to examine whether defensive investment and worker size are adjusted to local ecology in the only known bee with polymorphic workers, Tetragonisca angustula. Colonies of this species are defended by a morphologically specialized soldier caste. Our study included three populations that differed in the density of food competition and the occurrence of a parasitic robber bee. We found that colonies coexisting with robber bees had on average 43% more soldiers defending the nest entrance, while colonies facing stronger foraging competition had soldiers that were ~6–7% smaller. We then experimentally relocated colonies to areas with different levels of competition. When released from intense food competition, body sizes of guards and foragers increased. After introducing chemical robber bee cues at nest entrances, we found both a short-term and a long-term up-regulation of the number of soldiers defending the colony. Active soldier numbers remained high after the experiment for a duration equivalent to 2–3 worker life spans. How information about past parasite threat is stored in the colony is currently unknown. In summary, T. angustula adjusts both the number and the body size of active soldiers to local ecological conditions. Competitor density also affects forager (or minor) size, an important colony trait with potential community ecological consequences. Our study supports adaptive colony demography theory in a eusocial bee and highlights the importance of colony threats and competition as selective forces shaping colony phenotype.