Age-dependent perfume development in male orchid bees, Euglossa imperialis.

Male neotropical orchid bees concoct complex perfume blends by collecting exogenous volatiles from various sources, including orchids. These perfumes, stored in specialized hind-leg pouches and released during courtship, serve as inter-sexual signals. It has been hypothesized that male perfumes honestly indicate aspects of male fitness. If perfume traits such as quantity or complexity increase over individual lifetime, perfumes could reflect age (survival) and cumulative foraging success of males. We conducted a two-season mark-recapture study with Euglossa imperialis in Costa Rica, monitoring the balance of perfume uptake and expenditure over individual male lifetime. We sealed one hind-leg pouch upon initial capture, 'freezing' the perfume status on one side, and compared it with the other side at recapture to assess changes in perfume traits over time. Additionally, we used a novel method to estimate individual age by combining two parameters of wing degradation. Contrary to predictions, young to intermediate-aged bees had the highest quantities of perfume and the highest diversity of detected compounds. At the same time, the change in perfume between recaptures was positive (increase in amount and complexity) in young bees, whereas it was neutral to negative in older bees. Although these findings do not disprove an indicator function of male perfume, they shift the emphasis to non-cumulative fitness components such as sensory acuteness or cognitive capacity as likely targets of selection. Females preferring strong perfume signals in mates would maximize speed of foraging in offspring rather than their lifetime cumulative yield.

Function of environment-derived male perfumes in orchid bees.

Perfume making in male orchid bees is a unique behavior that has given rise to an entire pollination syndrome in the neotropics.1,2 Male orchid bees concoct and store species-specific perfume mixtures in specialized hind-leg pockets3 using volatiles acquired from multiple environmental sources, including orchid flowers.4,5 However, the function and the ultimate causes of this behavior have remained elusive.2,6 Although previous observations suggested that male perfumes serve as chemical signals, the attractiveness for females has not be shown.7,8 Here, we demonstrate that the possession of perfume increases male mating success and paternity in Euglossa dilemma, a species of orchid bees recently naturalized in Florida. We supplemented males reared from trap-nests with perfume loads harvested from wild conspecifics. In dual-choice experiments, males supplemented with perfumes mated with more females, and sired more offspring, than untreated, equal-aged, control males. Although perfume supplementation had little effect on the intensity of male courtship display, it changed the dynamics of male-male interactions. Our results demonstrate that male-acquired perfumes are sexual signals that stimulate females for mating and suggest that sexual selection is key in shaping the evolution of perfume communication in orchid bees.

Experimental disruption of social structure reveals totipotency in the orchid bee, Euglossa dilemma.

Eusociality has evolved multiple times across the insect phylogeny. Social insects with greater levels of social complexity tend to exhibit specialized castes with low levels of individual phenotypic plasticity. In contrast, species with simple social groups may consist of totipotent individuals that transition among behavioral and reproductive states. However, recent work has shown that in simple social groups, there can still be constraint on individual plasticity, caused by differences in maternal nourishment or social interaction. It is not well understood how these constraints arise, ultimately leading to the evolution of nonreproductive workers. Some species of orchid bees form social groups of a dominant and-one to two subordinate helpers where all individuals are reproductive. Females can also disperse to start their own nest as a solitary foundress, which includes a nonreproductive phase characterized by ovary inactivation, not typically expressed by subordinates. Little is known about individual flexibility across these trajectories. Here, using the orchid bee Euglossa dilemma, we assess the plasticity of subordinate helpers, finding that they are capable of the same behavioral, physiological, transcriptomic, and chemical changes seen in foundresses. Our results suggest that the lack of nonreproductive workers in E. dilemma is not due to a lack of subordinate plasticity.