The Impacts of Maturation and Experience on Volumetric Neuroplasticity in Solitary and Social Bees

Some animals are incredibly social, living and working together as one cohesive group. Alternatively, many animals are solitary, never living with and rarely interacting with others. A large body of biological research has focused on understanding the role that brains play in promoting these behavioral differences across species. Even so, it remains unclear why some brains facilitate social behavior while others do not. My dissertation aims to advance our understanding of this concept by characterizing bees’ brains and how they change over a lifetime. Bees are beneficial for investigating relationships between the brain and social behavior because some species are solitary while others are highly social. However, sociality in bees is more dynamic than that; a blending of these two extremes can also occur. This enables us to explore how brains change with social context within a single group of organisms. My first chapter uses a solitary bee to understand how simple social interactions can impact the brain. I found that—even in a solitary bee—certain brain regions grow in size in response to the presence of other bees. This trait may have been important in the evolutionary origins of social behavior. My second chapter investigated the effects of aging in the brains of two bee species, one that is sometimes social while the other is always social. I found that the brains of these species naturally change over time, a feature common to highly social species, e.g., honey bees. This suggests that having brains that change with age may be an important feature of sociality. My final research chapter made comparisons between queen and worker bees to investigate if their colony roles and behaviors dictated the relative size of different regions of their brains. I found that queen and worker brains respond differently to removing offspring care, a trait fundamental to defining their role in the colony. This highlights a potentially unique relationship between the brain and social life. Collectively, my dissertation used bees to enhance our understanding of what it means to have a social brain

Experience, but Not Age, is Associated With Volumetric Mushroom Body Expansion in Solitary Alkali Bees

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

Monitoring of Dung Beetle (Scarabaeidae and Geotrupidae) Activity Along Maryland\u27s Coastal Plain

Our understanding of how human activities impact insect communities is limited. Dung beetles, well known for the ecosystem services they provide, are faced with many conservation threats, particularly from deforestation and agriculture. Here we used 200-m transects and human-dung—baited pitfall traps to examine dung beetle populations in 7 forests of Maryland\u27s Coastal Plain. We set traps once a month, from May 2014 to April 2015, to determine species presence, abundance, range, and seasonality. We collected 6463 individuals representing 22 species; Janes Island State Park (JISP) had the highest abundance (2705 individuals) and Martinak State Park (MSP) had the highest species richness (19 species). During summer 2015, we examined the succession of dung beetles attracted to bait in JISP and MSP. We set 10 traps once a month (May–August) in each site and collected beetles on days 1, 3, 5, 7, 14, and 21 without dung replacement. In JISP, Onthophagus hecate (Scooped Scarab) was abundant throughout each 21-d period, and accounted for 68% of all beetles collected. In MSP, most specimens were collected by day 5. Here we provide information for conservation of locally rare or uncommon species

Age-Related Mushroom Body Expansion in Male Sweat Bees and Bumble Bees

A well-documented phenomenon among social insects is that brain changes occur prior to or at the onset of certain experiences, potentially serving to prime the brain for specific tasks. This insight comes almost exclusively from studies considering developmental maturation in females. As a result, it is unclear whether age-related brain plasticity is consistent across sexes, and to what extent developmental patterns differ. Using confocal microscopy and volumetric analyses, we investigated age-related brain changes coinciding with sexual maturation in the males of the facultatively eusocial sweat bee, Megalopta genalis, and the obligately eusocial bumble bee, Bombus impatiens. We compared volumetric measurements between newly eclosed and reproductively mature males kept isolated in the lab. We found expansion of the mushroom bodies—brain regions associated with learning and memory—with maturation, which were consistent across both species. This age-related plasticity may, therefore, play a functionally-relevant role in preparing male bees for mating, and suggests that developmentally-driven neural restructuring can occur in males, even in species where it is absent in females

Tracing Brain Structures of Alkali Bees to Investigate Endocrine and Social Effects on Neural Plasticity

For highly social bee species, juvenile hormone (JH) and social cues are linked to increased expression of class-based social features. However, little data has been collected on the relationship between these variables and homologous features in non-social bees. To fill this gap in data, we studied the neuroanatomical response of Nomia melanderi, a non-social bee species, to endocrine and social treatments. Since N. melanderi is a non-social bee with pre-adaptations to sociality, such as brood care and aggregative nesting habits, its responses to hormone treatment and social cues can be used to model how neural plasticity in non-social ancestors of highly social bee species may have played a role in social evolution. Specifically, we measured volumetric difference in mushroom body structures, which are known to function in social cognition in social bees, in response to our treatments. Brains from the six treatment groups were dissected and imaged using confocal microscopy techniques. By scaling the actual distance in an image to its pixel density, reliable measurements of volume are produced from evenly spaced cross-sections of N. melanderi brain. Since data collection for the current phase of the project is still underway, it’s premature to make any conclusion about how JH and social cues influence neural plasticity in N. melanderi. However, the results of our experiment are likely to provide unique insights into the evolution of sociality in bee species generally.

DataSheet3_Maternal body condition and season influence RNA deposition in the oocytes of alfalfa leafcutting bees (Megachile rotundata).xlsx

Maternal effects are an important source of phenotypic variance, whereby females influence offspring developmental trajectory beyond direct genetic contributions, often in response to changing environmental conditions. However, relatively little is known about the mechanisms by which maternal experience is translated into molecular signals that shape offspring development. One such signal may be maternal RNA transcripts (mRNAs and miRNAs) deposited into maturing oocytes. These regulate the earliest stages of development of all animals, but are understudied in most insects. Here we investigated the effects of female internal (body condition) and external (time of season) environmental conditions on maternal RNA in the maturing oocytes and 24-h-old eggs (24-h eggs) of alfalfa leafcutting bees. Using gene expression and WGCNA analysis, we found that females adjust the quantity of mRNAs related to protein phosphorylation, transcriptional regulation, and nuclease activity deposited into maturing oocytes in response to both poor body condition and shorter day lengths that accompany the late season. However, the magnitude of these changes was higher for time of season. Females also adjusted miRNA deposition in response to seasonal changes, but not body condition. We did not observe significant changes in maternal RNAs in response to either body condition or time of season in 24-h eggs, which were past the maternal-to-zygotic transition. Our results suggest that females adjust the RNA transcripts they provide for offspring to regulate development in response to both internal and external environmental cues. Variation in maternal RNAs may, therefore, be important for regulating offspring phenotype in response to environmental change.</p

DataSheet10_Maternal body condition and season influence RNA deposition in the oocytes of alfalfa leafcutting bees (Megachile rotundata).pdf

Maternal effects are an important source of phenotypic variance, whereby females influence offspring developmental trajectory beyond direct genetic contributions, often in response to changing environmental conditions. However, relatively little is known about the mechanisms by which maternal experience is translated into molecular signals that shape offspring development. One such signal may be maternal RNA transcripts (mRNAs and miRNAs) deposited into maturing oocytes. These regulate the earliest stages of development of all animals, but are understudied in most insects. Here we investigated the effects of female internal (body condition) and external (time of season) environmental conditions on maternal RNA in the maturing oocytes and 24-h-old eggs (24-h eggs) of alfalfa leafcutting bees. Using gene expression and WGCNA analysis, we found that females adjust the quantity of mRNAs related to protein phosphorylation, transcriptional regulation, and nuclease activity deposited into maturing oocytes in response to both poor body condition and shorter day lengths that accompany the late season. However, the magnitude of these changes was higher for time of season. Females also adjusted miRNA deposition in response to seasonal changes, but not body condition. We did not observe significant changes in maternal RNAs in response to either body condition or time of season in 24-h eggs, which were past the maternal-to-zygotic transition. Our results suggest that females adjust the RNA transcripts they provide for offspring to regulate development in response to both internal and external environmental cues. Variation in maternal RNAs may, therefore, be important for regulating offspring phenotype in response to environmental change.</p

DataSheet4_Maternal body condition and season influence RNA deposition in the oocytes of alfalfa leafcutting bees (Megachile rotundata).xlsx

Maternal effects are an important source of phenotypic variance, whereby females influence offspring developmental trajectory beyond direct genetic contributions, often in response to changing environmental conditions. However, relatively little is known about the mechanisms by which maternal experience is translated into molecular signals that shape offspring development. One such signal may be maternal RNA transcripts (mRNAs and miRNAs) deposited into maturing oocytes. These regulate the earliest stages of development of all animals, but are understudied in most insects. Here we investigated the effects of female internal (body condition) and external (time of season) environmental conditions on maternal RNA in the maturing oocytes and 24-h-old eggs (24-h eggs) of alfalfa leafcutting bees. Using gene expression and WGCNA analysis, we found that females adjust the quantity of mRNAs related to protein phosphorylation, transcriptional regulation, and nuclease activity deposited into maturing oocytes in response to both poor body condition and shorter day lengths that accompany the late season. However, the magnitude of these changes was higher for time of season. Females also adjusted miRNA deposition in response to seasonal changes, but not body condition. We did not observe significant changes in maternal RNAs in response to either body condition or time of season in 24-h eggs, which were past the maternal-to-zygotic transition. Our results suggest that females adjust the RNA transcripts they provide for offspring to regulate development in response to both internal and external environmental cues. Variation in maternal RNAs may, therefore, be important for regulating offspring phenotype in response to environmental change.</p

DataSheet2_Maternal body condition and season influence RNA deposition in the oocytes of alfalfa leafcutting bees (Megachile rotundata).xlsx

Maternal effects are an important source of phenotypic variance, whereby females influence offspring developmental trajectory beyond direct genetic contributions, often in response to changing environmental conditions. However, relatively little is known about the mechanisms by which maternal experience is translated into molecular signals that shape offspring development. One such signal may be maternal RNA transcripts (mRNAs and miRNAs) deposited into maturing oocytes. These regulate the earliest stages of development of all animals, but are understudied in most insects. Here we investigated the effects of female internal (body condition) and external (time of season) environmental conditions on maternal RNA in the maturing oocytes and 24-h-old eggs (24-h eggs) of alfalfa leafcutting bees. Using gene expression and WGCNA analysis, we found that females adjust the quantity of mRNAs related to protein phosphorylation, transcriptional regulation, and nuclease activity deposited into maturing oocytes in response to both poor body condition and shorter day lengths that accompany the late season. However, the magnitude of these changes was higher for time of season. Females also adjusted miRNA deposition in response to seasonal changes, but not body condition. We did not observe significant changes in maternal RNAs in response to either body condition or time of season in 24-h eggs, which were past the maternal-to-zygotic transition. Our results suggest that females adjust the RNA transcripts they provide for offspring to regulate development in response to both internal and external environmental cues. Variation in maternal RNAs may, therefore, be important for regulating offspring phenotype in response to environmental change.</p

DataSheet7_Maternal body condition and season influence RNA deposition in the oocytes of alfalfa leafcutting bees (Megachile rotundata).xlsx

Maternal effects are an important source of phenotypic variance, whereby females influence offspring developmental trajectory beyond direct genetic contributions, often in response to changing environmental conditions. However, relatively little is known about the mechanisms by which maternal experience is translated into molecular signals that shape offspring development. One such signal may be maternal RNA transcripts (mRNAs and miRNAs) deposited into maturing oocytes. These regulate the earliest stages of development of all animals, but are understudied in most insects. Here we investigated the effects of female internal (body condition) and external (time of season) environmental conditions on maternal RNA in the maturing oocytes and 24-h-old eggs (24-h eggs) of alfalfa leafcutting bees. Using gene expression and WGCNA analysis, we found that females adjust the quantity of mRNAs related to protein phosphorylation, transcriptional regulation, and nuclease activity deposited into maturing oocytes in response to both poor body condition and shorter day lengths that accompany the late season. However, the magnitude of these changes was higher for time of season. Females also adjusted miRNA deposition in response to seasonal changes, but not body condition. We did not observe significant changes in maternal RNAs in response to either body condition or time of season in 24-h eggs, which were past the maternal-to-zygotic transition. Our results suggest that females adjust the RNA transcripts they provide for offspring to regulate development in response to both internal and external environmental cues. Variation in maternal RNAs may, therefore, be important for regulating offspring phenotype in response to environmental change.</p