FoxP in bees: A comparative study on the developmental and adult expression pattern in three bee species considering isoforms and circuitry

Abstract

Mutations in the transcription factors FOXP1, FOXP2, and FOXP4 affect human cognition, including language. The FoxP gene locus is evolutionarily ancient and highly conserved in its DNA-binding domain. In Drosophila melanogaster FoxP has been implicated in courtship behavior, decision making, and specific types of motor-learning. Because honeybees (Apis mellifera, Am) excel at navigation and symbolic dance communication, they are a particularly suitable insect species to investigate a potential link between neural FoxP expression and cognition. We characterized two AmFoxP isoforms and mapped their expression in the brain during development and in adult foragers. Using a custom-made antiserum and in situ hybridization, we describe 11 AmFoxP expressing neuron populations. FoxP was expressed in equivalent patterns in two other representatives of Apidae; a closely related dwarf bee and a bumblebee species. Neural tracing revealed that the largest FoxP expressing neuron cluster in honeybees projects into a posterior tract that connects the optic lobe to the posterior lateral protocerebrum, predicting a function in visual processing. Our data provide an entry point for future experiments assessing the function of FoxP in eusocial Hymenoptera.

Kenyon Cell Subtypes/Populations in the Honeybee Mushroom Bodies: Possible Function Based on Their Gene Expression Profiles, Differentiation, Possible Evolution, and Application of Genome Editing

“…They also reported FoxP expression in the honeybee MBs (Schatton and Scharff, 2017 ). These findings suggest that neural populations with FoxP expression that are related to reinforcement-based learning abilities are conserved among animal species (Schatton and Scharff, 2017 ; Schatton et al, 2018 ).…”

“…Recently, Schatton and Scharff ( 2017 ); Schatton et al ( 2018 ) identified a novel KC population expressing transcription factor FoxP in the MBs of the honeybee brain (Figure 1D ) (Schatton and Scharff, 2017 ; Schatton et al, 2018 ). Although Kiya et al ( 2008 ), who first reported the FoxP expression in the honeybee brain, detected no significant FoxP expression in the honeybee MBs (Kiya et al, 2008 ), Schatton et al notified that, in Drosophila , a MB-core subpopulation expresses FoxP , which is related to decision-making (DasGupta et al, 2014 ).…”

“…The expression of Syt14 and dlg5 becomes detectable at the middle pupal stages (around P3), and is restricted to the lKCs at the adult stage, suggesting that expression of Syt14 and dlg5 is characteristic of differentiated lKCs (Suenami et al, 2016 ). The FoxP expression is also not detected in larval MBs, but becomes detectable in the MBs at the middle-to-late pupal stages (P4-5) (Schatton et al, 2018 ), suggesting that FoxP expression is also characteristic of differentiated KCs. In contrast, KCs expressing mKast become detectable at the late pupal stages (P7 and P8) (Kaneko et al, 2013 ), suggesting that mKCs develop after the lKCs begin to differentiate or mKast is expressed at the late stage of mKC differentiation.…”

Identification of the neurotransmitter profile of AmFoxP expressing neurons in the honeybee brain using double-label in situ hybridization

“…Invertebrate genomes harbor only one FoxP gene locus that contains a highly conserved DNA-binding domain [ 24 , 25 ]. In sponges FoxP is upregulated in vitro during the formation of cell aggregates [ 26 ].…”

“…In Drosophila , FoxP (dFoxP) has been implicated in decision-making, locomotion and motor learning [ 27 – 30 ]. In honeybees, FoxP (AmFoxP) is expressed in the cortical areas of all major neuropils, either in dense neuron clusters or more widely dispersed neuron groups [ 25 , 31 , 32 ]. The FoxP gene is most similar to vertebrate FoxP1 , based on particular alternative splice forms in bilaterians [ 25 , 33 ].…”