A genetic switch for worker nutrition-mediated traits in honeybees

Abstract

Highly social insects are characterized by caste dimorphism, with distinct size differences of reproductive organs between fertile queens and the more or less sterile workers. An abundance of nutrition or instruction via diet-specific compounds has been proposed as explanations for the nutrition-driven queen and worker polyphenism. Here, we further explored these models in the honeybee (Apis mellifera) using worker nutrition rearing and a novel mutational screening approach using the clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 (CRISPR/Cas9) method. The worker nutrition-driven size reduction of reproductive organs was restricted to the female sex, suggesting input from the sex determination pathway. Genetic screens on the sex determination genes in genetic females for size polyphenism revealed that doublesex (dsx) mutants display size-reduced reproductive organs irrespective of the sexual morphology of the organ tissue. In contrast, feminizer (fem) mutants lost the response to worker nutrition-driven size control. The first morphological worker mutants in honeybees demonstrate that the response to nutrition relies on a genetic program that is switched “ON” by the fem gene. Thus, the genetic instruction provided by the fem gene provides an entry point to genetically dissect the underlying processes that implement the size polyphenism.

Developmental plasticity shapes social traits and selection in a facultatively eusocial bee

“…Gene networks that regulate developmental plasticity may be a nexus of such regulatory changes that enable the evolution of social traits from ancient genes. Many of the genes underlying social behavior in insects respond to variable developmental conditions (e.g., diet, aggression, hormone levels) to produce adults with different behavioral traits (e.g., workers, queens) (32)(33)(34)(35)(36). Accordingly, the leading hypotheses proposed to explain how eusociality evolves from a solitary ancestor evoke developmental processes as a source of initial phenotypic variation for traits related to social behavior.…”

Development of a film-assisted honeybee egg collection system (FECS)

“…For any researcher with average experience in beekeeping and microinjection, the number of eggs collected by FECS would be enough for any subsequent procedures and at least would not be a limiting factor in successful honeybee genome editing. Recently, Roth et al (2019) have shown one-step honeybee genome editing protocol which allows phenotype observation without subsequent screening and mating (Roth et al 2019). However, there are many phenotypes that can only be measured from substantial numbers of mutants such as social behaviors and resistance to stress factors.…”

Genetics of Social Behavior

“…Finally, with both traditional and newly developed genetic approaches, researchers have begun to experimentally manipulate candidate genes to confirm their effects on social behavior [14,16]. Because the genetic bases of social behavior are apparently very complex, these experimental studies, which are typically limited to one or a few genes that are a priori of interest, will need to be coupled with the unbiased approaches described above in order to gain a full understanding of the genetic basis and evolution of social behavior.…”