Sociality emerges from solitary behaviours and reproductive plasticity in the orchid beeEuglossa dilemma

Abstract

The evolution of eusociality and sterile worker castes represents a major transition in the history of life. Despite this, little is known about the mechanisms involved in the initial transition from solitary to social behaviour. It has been hypothesized that plasticity from ancestral solitary life cycles was coopted to create queen and worker castes in insect societies. Here, we tested this hypothesis by examining gene expression involved in the transition from solitary to social behaviour in the orchid bee Euglossa dilemma . To this end, we conducted observations that allowed us to classify bees into four distinct categories of solitary and social behaviour. Then, by sequencing brain and ovary transcriptomes from these behavioural phases, we identified gene expression changes overlapping with socially associated genes across multiple eusocial lineages. We find that genes involved in solitary E. dilemma ovarian plasticity overlap extensively with genes showing differential expression between fertile and sterile workers—or between queens and workers in other eusocial bees. We also find evidence that sociality in E. dilemma reflects gene expression patterns involved in solitary foraging and non-foraging nest care behaviours. Our results provide strong support for the hypothesis that eusociality emerges from plasticity found across solitary life cycles.

Transcriptomic Signatures of Ageing Vary in Solitary and Social Forms of an Orchid Bee

“…In social subordinate females, surprisingly, functions related to egg production were upregulated in young individuals. Subordinate females of this species, unlike sterile workers of highly eusocial species, have been reported to lay eggs, although the dominant female systematically replaces subordinate eggs with her own ( Saleh and Ramírez 2019 ). Other pathways which were enriched among age-related genes in subordinate females were mainly linked to metabolism (e.g., lipid metabolic process, fructose 6-phosphate metabolic process), which may reflect the metabolically costly behaviors carried out by this caste (foraging and nest defense, Boff et al 2015 ).…”

“…Interestingly, these functions were upregulated with age, suggesting that solitary females invest more in somatic repair as they get older. This may reflect the shift in behavior which solitary females undergo with age in this species, as young foundress females may invest more in reproduction and metabolically costly tasks related to nest construction, whereas older solitary females are primarily guarding their brood inside the nest ( Saleh and Ramírez 2019 ) and may therefore be able to invest more in somatic maintenance.…”

Transcriptomic signatures of ageing vary in solitary and social forms of an orchid bee

“…Genes relating to metabolic activities appear to be upregulated in young rather than old solitary females, suggesting that high metabolic activity early in life may increase senescence, as predicted by the free radical theory of ageing (Harman 1982). In the cryptic sister species Euglossa dilemma, young foundress females indeed spend more time foraging for brood provisions, a metabolically costly task, compared to when they later enter the "guard phase", during which they stay in the nest, guarding their brood cells (Saleh and Ramírez 2019). Interestingly, genes directly related to the oxidative metabolism of various substrates, notably lipids (cytochrome P450, cytochrome b5) are upregulated with age in solitary females.…”

“…Another factor which may explain the lack of ageing signs in dominant females is the ingestion of subordinate-laid eggs by dominant females. Video recordings of E. dilemma nests revealed that oophagy, whereby the dominant female ingests eggs laid by subordinate females in her nest to replace them with her own, occurs commonly in this species (Saleh and Ramírez 2019). If this behaviour also occurs in the closely related E. viridissima, this could constitute a notable nutritional source for dominant females, thereby reducing any trade-off generated by the allocation of limited resources.…”

“…An alternative explanation for the differences in gene expression with age observed in the solitary, but not observed in the social females is a potential shift in behaviour with age in the solitary females. It has been proposed for the sister species E. dilemma that transcriptomic shifts throughout the solitary phases of the life cycle may be attributed to a shift in behaviour, as the female goes from an actively foraging foundress to a relatively inactive guard, caring for her brood (Saleh and Ramírez 2019). Similar to the differences observed between young and old solitary females in our study species E. viridissima, Saleh and Ramirez (2019) found that metabolic pathways were upregulated in foundresses compared to females in the guarding phase.…”