Evolutionary dynamics of mushroom body Kenyon cell types in hymenopteran brains from multifunctional type to functionally specialized types

Abstract

Evolutionary dynamics of diversification of brain neuronal cell types that have underlain behavioral evolution remain largely unknown. Here, we compared transcriptomes and functions of Kenyon cell (KC) types that compose the mushroom bodies between the honey bee and sawfly, a primitive hymenopteran insect whose KCs likely have the ancestral properties. Transcriptome analyses show that the sawfly KC type shares some of the gene expression profile with each honey bee KC type, although unique gene expression profiles have also been acquired in each honey bee KC type. In addition, functional analysis of two sawfly genes suggested that the functions in learning and memory of the ancestral KC type were heterogeneously inherited among the KC types in the honey bee. Our findings strongly suggest that the functional evolution of KCs in Hymenoptera involved two previously hypothesized processes for evolution of cell function: functional segregation and divergence.

Multiple molecular links between the circadian clock and memory centers in honey bees

“…The sKC cell bodies are closely arranged at the inner core of the MB calyces, and this area is visually distinguishable from that of the lKCs ( 20 ). We dissected the sKCs of all four MB calyces of one brain using LCM and pooled the RNA samples from 11-12 brains to yield high-quality RNA. For each of the 7 different collection times, we collected two replicates each from two different colonies for RNA-sequencing [RNA-seq (Fig.…”

“…That the area showing co-expression expanded from few KCs to ( The respective KC areas were identified by DAPI staining. (G) Schematic representation of KC sub-types (11) and highlighted in orange, pink, and blue the expansion of preferential co-exp. from sKCs to more KCs (sKCs + mKCs) to all KCs (sKCs + mKCs + lKCs) except foxP + region (fig.…”

“…However, how signals from the clock and sensory systems are combined and consolidated in memory cells is still unclear. Here, we used social honey bees which have elaborated mushroom bodies (MBs), the major insect memory centers ( 11 ), and show an exceptional capability to form multiple time-memories under free-flight conditions ( 12,13 ) to search for candidate molecular interactions between the clock and memory centers. Our project was motivated by an earlier study from our lab showing that expression of the neuronal-activity regulated transcription factor (TF) Egr1 in the small Kenyon cells (sKCs), the major multimodal neuronal population of the MBs, correlates with training-time ( 14,15 ).…”

Insights from the past: the work of Hans von Alten on the evolution of brain structure, ecological adaptation, and cognition in hymenopteran species

“…In a recent extension of these studies, the same research group, Kuwabara et al (2023) , performed comparative transcriptome analyses on Kenyon cell types in the honeybee and the turnip sawfly ( Athalia rosae , Tenthredinidae), a primitive flying Hymenoptera without central-place foraging habits. These analyses revealed both similar and different gene expression between these two species.…”

Unique spatially and temporary-regulated/sex-specific expression of a long ncRNA, Nb-1, suggesting its pleiotropic functions associated with honey bee lifecycle

“…The honey bee workers inform their nestmate of the memorized location of the food source using ‘dance communication’ 12 , 13 and have been used as a model for the study of advanced brain functions 14 . The mushroom bodies (MBs) are a higher-order center of memory, learning, and sensory integration of the insect brain 16 – 18 , and the MBs of aculeate species, including the honey bee, are more elaborate when compared with those of primitive hymenopteran species 19 – 21 . Furthermore, neural activity is induced in the worker honey bee MBs after foraging flights, suggesting a role in information processing during the foraging flights 22 – 25 .…”