Experience, but not age, is associated with volumetric mushroom body expansion in solitary alkali bees

Abstract

In social insects, changes in behavior are often accompanied by structural changes in the brain. This neuroplasticity may come with experience (experience-dependent) or age (experience-expectant). Yet, the evolutionary relationship between neuroplasticity and sociality is unclear, because we know little about neuroplasticity in the solitary relatives of social species. We used confocal microscopy to measure brain changes in response to age and experience in a solitary halictid bee (Nomia melanderi). First, we compared the volume of individual brain regions among newly-emerged females, laboratory females deprived of reproductive and foraging experience, and free-flying, nesting females. Experience, but not age, led to significant expansion of the mushroom bodies—higher-order processing centers associated with learning and memory. Next, we investigated how social experience influences neuroplasticity by comparing the brains of females kept in the laboratory either alone or paired with another female. Paired females had significantly larger olfactory regions of the mushroom bodies. Together, these experimental results indicate that experience-dependent neuroplasticity is common to both solitary and social taxa, whereas experience-expectant neuroplasticity may be an adaptation to life in a social colony. Further, neuroplasticity in response to social chemical signals may have facilitated the evolution of sociality.

Reduced neural investment in post-reproductive females of the bee Ceratina calcarta

“… 19 ) are required to determine to what extent brain development between the newly emerged daughter and foundress stages is age vs. experience dependent. While our study was not designed to explicitly test for experience-expectant plasticity, this result is consistent with the two other studies of solitary bees which showed no experience-expectant plasticity 19 , 23 .…”

“…Workers instead accrue indirect fitness by helping the colony reproduce throughout their lives. The only studies to examine the development of brain structures of solitary or small-colony bees either used individuals still engaged in reproduction 15 , 18 , 23 , 28 or tropical species with no distinct end to the reproductive season 27 , 31 . Likewise, studies demonstrating experience-based enlargement of the MB in Lepidoptera also did not include post-reproductive individuals 13 , 14 , 51 .…”

“…In the ant Camponotus floridanus, socially isolated individuals had smaller MB calyces than ants in a social nest 22 . The solitary bee Nomia melanderi showed increased growth in the lip region of the MB calyx when experimentally paired with another bee 23 . In some species of bees and paper wasps social dominance of reproductive queens over subordinate workers, rather than social interactions themselves, result in increased MB calyx volume of social dominants relative to subordinates 12 , 15 , 24 – 26 .…”

“…These are all species that live in social groups where young workers do not need to begin foraging immediately. Data are mixed on whether experience-expectant plasticity occurs in the facultatively social and solitary sweat bee Megalopta genalis 27 , 31 , but experience-expectant plasticity was not found in the only two species of solitary bees in which it was investigated 19 , 23 .…”

Age-related mushroom body expansion in male sweat bees and bumble bees

“…Future work comparing sex-specific patterns of brain development in additional bee species is needed to determine the pervasiveness of intersexual differences in neuroplasticity. Investigating socioecological drivers of neuroplasticity in both sexes, particularly in solitary species where females lack age-related plasticity 57 , 58 , will provide a more robust understanding of the relationship between neuroplasticity and social evolution.…”