Biology subjects

Bloch, G.

Publications and source records attributed to Bloch, G..

10 recordsLinked to original sources

bioRxiv2024

Data-driven analyses of social complexity in bees reveal phenotypic diversification following a major evolutionary transition

How social complexity evolved is a long-standing enigma. In most animal groups, social complexity is typically classified into a few discrete classes. This approach is oversimplified and constrains our inference of social evolution to a narrow trajectory consisting of transitions between classes. This approach also limits quantitative studies on the molecular and environmental drivers of social complexity. However, the recent accumulation of relevant quantitative data has now set the stage to overcome these limitations. Here, we propose a data-driven approach for studying the full diversity of social phenotypes. We curated and analyzed a comprehensive dataset encompassing 17 social traits for 77 species and studied the evolution of social complexity in bees. We found that corbiculate bees -- honey bees, stingless bees, and bumble bees -- underwent a major evolutionary transition [~]70 mya, which is inconsistent with the stepwise progression of the social ladder conceptual framework. This major evolutionary transition was followed by a phase of substantial phenotypic diversification of social complexity. Non-corbiculate bee lineages display a continuum of social complexity, ranging from solitary to simple societies, but do not reach levels of social complexity comparable to those of corbiculate bees. Bee evolution provides a unique demonstration of a macroevolutionary process in which a major transition removed biological constraints and opened novel evolutionary opportunities, driving the exploration of the landscape of social phenotypes. Our approach can be extended to incorporate additional data types and readily applied to illuminate the evolution of social complexity in additional animal groups.

evolutionary biology↗

bioRxiv2023

Bumble bees (Bombus terrestris) use time-memory to associate reward with color and time of day

Circadian clocks regulate ecologically important complex behaviors in honey bees but it is not clear to what extent these observations can be extended to other species of bees. One key behavior is time-memory allowing foraging bees to precisely time flower visitation to periods of maximal pollen or nectar availability and reducing the costs of arriving at a flower patch at the wrong time. It is unclear whether other bees such as bumble bees, who live in smaller societies and forage over shorter distances than honey bees, can similarly associate a reward with time of day. We trained individually marked bumble bee (Bombus terrestris) workers to forage for sugar syrup in a flight cage with yellow or blue feeders rewarding either during the morning or evening. After a two-weeks training session, we recorded all visitations to colored feeders filled with only water. We repeated this experiment twice, with different colonies. We found that bees tended to show higher foraging activity during the morning and evening training sessions compared to other times during the day. Trained bees were more likely to visit feeders with colors rewarding compared to non-rewarding at the same time of day during the training sessions and with relatively fewer mistakes. Our findings lend credence to the hypothesis that efficient time-memory is not limited to species such as honey bees that evolved sophisticated social foraging behaviors over large distances.

animal behavior and cognition↗

bioRxiv2020

Juvenile hormone affects the development and strength of circadian rhythms in young bumble bee (Bombus terrestris) workers

The circadian and endocrine systems influence many physiological processes in animals, but little is known on the ways they interact in insects. We tested the hypothesis that juvenile hormone (JH) influences circadian rhythms in the social bumble bee Bombus terrestris. JH is the major gonadotropin in this species coordinating processes such as vitellogenesis, oogenesis, wax production, and behaviors associated with reproduction. It is unknown however, whether it also influences circadian processes. We topically treated newly-emerged bees with the allatoxin Precocene-I (P-I) to reduce circulating JH titers and applied the natural JH (JH-III) for replacement therapy. We repeated this experiment in three trials, each with bees from different source colonies. Measurements of ovarian activity confirmed that our JH manipulations were effective; bees treated with P-I had inactive ovaries, and this effect was fully reverted by subsequent JH treatment. We found that JH augments the strength of circadian rhythms and the pace of rhythm development in individually isolated newly emerged worker bees. JH manipulation did not affect the free-running circadian period, overall level of locomotor activity, or the amount of sleep. Given that acute manipulation at an early age produced relatively long-lasting effects, we propose that JH effect on circadian rhythms is mostly organizational, accelerating the development or integration of the circadian system.

animal behavior and cognition↗

bioRxiv2020

Is diversity in worker body size important for the performance of bumble bee colonies?

Specialization and plasticity are important for many forms of collective behavior, but the interplay between these factors is little understood. In insect societies, workers are often predisposed to specialize in different tasks, sometimes with morphological or physiological adaptations, facilitating a division of labor. Workers may also plastically switch between tasks or vary their effort. The degree to which predisposed specialization limits plasticity is not clear and has not been systematically tested in ecologically relevant contexts. We addressed this question in 20 freely-foraging bumble bee (Bombus terrestris) colonies by continually manipulating colonies to contain either a typically diverse or reduced ("homogeneous") worker body size distribution, over two trials. Pooling both trials, diverse colonies did better in several indices of colony performance. The importance of body size was further demonstrated by the finding that foragers were larger than nurses even in homogeneous colonies with a very narrow body size range. However, the overall effect of size diversity stemmed mostly from one trial. In the other trial, homogeneous and diverse colonies showed comparable performance. By comparing behavioral profiles based on several thousand observations, we found evidence that workers in homogeneous colonies in this trial rescued colony performance by plastically increasing behavioral specialization and/or individual effort, compared to same-sized individuals in diverse colonies. Our results are consistent with a benefit to colonies of predisposed (size-diverse) specialists under certain conditions, but also suggest that plasticity or effort, can compensate for reduced (size-related) specialization. Thus, we suggest that an intricate interplay between specialization and plasticity is functionally adaptive in bumble bee colonies.

animal behavior and cognition↗

bioRxiv2020

The evolution of extreme fertility defied ancestral gonadotropin mediated brain-reproduction tradeoff

Gonadotropic hormones coordinate processes in diverse tissues regulating animal reproductive physiology and behavior. Juvenile hormone (JH) is the ancient and most common gonadotropin in insects, but not in advanced eusocial honey bees and ants. To probe the evolutionary basis of this change, we combined endocrine manipulations, transcriptomics, and behavioral analyses to study JH regulated processes in a bumble bee showing an intermediate level of sociliality. We found that in the fat body, more JH-regulated genes were upregulated and enriched for metabolic and biosynthetic pathways. This transcriptomic pattern is consistent with earlier evidence that JH is the major gonadotropin in the bumble bee. In the brain, most JH-regulated genes were downregulated and enriched for protein turnover pathways. Brain ribosomal protein gene expression was similarly downregulated in dominant workers, which naturally have high JH titers. In other species, similar downregulation of protein turnover is found in aging brains or under stress, and is associated with compromised long-term memory and health. These findings suggest a previously unknown gonadotropin-mediated tradeoff. We did not find a similar downregulation of protein turnover pathways in the brain of honey bees in which JH is not a gonadotropin but rather regulates division of labor. These differences between JH effets in the bumble bee and in the advanced eusocial honey bee suggest that the evolution of advanced eusociality was associated with modifications in hormonal signaling supporting extended and extremely high fertility while reducing the ancient costs of high gonadotropin titers to the brain.

evolutionary biology↗

bioRxiv2019

Colony volatiles and substrate-borne vibrations entrain circadian rhythms and are potential mediators of social synchronization in honey bee colonies

Internal circadian clocks organize animal behavior and physiology and are entrained by ecologically-relevant external time-givers such as light and temperature cycles. In the highly social honey bee, social time-givers are important and can override photic entrainment, but the cues mediating social synchronization are unknown. Here we tested whether substrate-borne vibrations and hive volatiles can mediate social synchronization in honey bees. We first placed newly-emerged worker bees on the same or on a different substrate on which we placed cages with foragers entrained to ambient day- night cycles, while minimizing transfer of volatiles between cages. In the second experiment, we exposed young bees to constant airflow coming from either a free-foraging colony or a similar size control hive containing only empty combs, while minimizing transfer of substrate-borne vibrations between cages. After five days, we individually isolated each focal bee in an individual cage in an environmental chamber, and monitored locomotor activity. We repeated each experiment five times, each trail with bees from a different source colony, monitoring a total of more than 1000 bees representing diverse genotypes. We found that bees placed on the same substrate as foragers showed a stronger phase coherence; and in 3 of 5 trials their phase was more similar to that of foragers, compared to bees placed on a different substrate. In the second experiment, bees exposed to air from a colony showed a stronger phase coherence, and in 4 out of 5 trial their phase was more similar to that of foragers, compared to control bees exposed to air from an empty hive. These findings lend credence to the hypothesis that surrogates of activity such as substrate-borne vibrations, and volatile cues entrain circadian rhythms in natural free-foraging honey bee colonies.

animal behavior and cognition↗

bioRxiv2019

Brain microRNA expression associated with social evolution in bees

Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific changes in gene expression, but the key nodes that drive these regulatory changes are unknown. We examined the relationship between social organization and lineage-specific microRNAs (miRNAs). Genome scans across 12 bee species showed that miRNA copy-number is mostly conserved and not associated with sociality. However, deep sequencing of small RNAs in six bee species revealed a substantial proportion (20-35%) of detected miRNAs had lineage-specific expression in the brain, 24-72% of which did not have homologs in other species. Lineage-specific miRNAs disproportionately target lineage-specific genes, and have lower expression levels than shared miRNAs. The predicted targets of lineage-specific miRNAs are not enriched for genes with caste-biased expression or genes under positive selection in social species. Together, these results suggest that novel miRNAs may coevolve with novel genes, and thus contribute to lineage-specific patterns of evolution in bees, but do not appear to have significant influence on social evolution. Our analyses also support the hypothesis that many new miRNAs are purged by selection due to deleterious effects on mRNA targets, and suggest genome structure is not as influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs.

genomics↗

bioRxiv2019

Worker body size but not its age influences phototaxis in a bumblebee (Bombus terrestris, L.)

We studied phototaxis, the directional movement relative to light, in the bumble bee Bombus terrestris. We first developed and validated a MATLAB based system enabling reliable high-resolution tracking of a bee and a measurement of her distance relative to a changing LED light source. Using this system we found in all our experiments that workers show positive phototaxis. The strength of the phototactic response was influenced by body size but not age, and this effect was significant when the light source was weak. In a separate experiment, foragers showed stronger phototactic response compared to nurses only in one of two trials in which they were larger and tested with weak light intensity. The evidence that phototaxis is associated with size-based division of labor in the bumble bee and with age-related division of labor in the honey bee, lends credence to response threshold models implicating the response to light in the organization of division of labor in cavity dwelling social insects.

animal behavior and cognition↗

bioRxiv2019

Juvenile hormone interacts with multiple factors to modulate aggression and dominance in a social bumblebee

Juvenile hormone (JH) is a key regulator of insect development and reproduction. Given that JH commonly affects adult insect fertility, it has been hypothesized to also regulate behaviors such as dominance and aggression that are associated with reproduction. We tested this hypothesis in the bumble bee Bombus terrestris for which JH has been shown to be the major gonadotropin. We used the allatoxin Precocene-I (P-I) to reduce hemolymph JH titers and replacement therapy with the natural JH to revert this effect. In small orphan groups of workers with similar body size but mixed treatment, P-I treated bees showed lower aggressiveness, oogenesis, and dominance rank compared with control and replacement therapy treated bees. In similar groups in which all bees were treated similarly, there was a clear dominance hierarchy, even in P-I and replacement therapy treatment groups in which the bees showed similar levels of ovarian activation. In a similar experiment in which bees differed in body size, larger bees were more likely to be dominant despite their similar JH treatment and ovarian state. In the last experiment, we show that JH manipulation does not affect dominance rank in groups that had already established a stable dominance hierarchy. These findings solve previous ambiguities concerning whether or not JH affects dominance in bumble bees. JH positively affects dominance, but bees with similar levels of JH can nevertheless establish dominance hierarchies. Thus, multiple factors including JH, body size, and previous experience affect dominance and aggression in social bumble bees.

animal behavior and cognition↗

bioRxiv2018

Signals from the brood modulate the sleep of brood tending bumblebee workers

Sleep is ubiquitous in vertebrates and invertebrates, and its chronic lost is typically associated with reduced performance, health, or survival. Nevertheless, some animals can give up sleep in order to increase survival or mating opportunities. We studied the interplay between sleep and brood care in the social bumblebee Bombus terrestris. We first used video recording and detailed behavioral analyses to confirm that the bumblebee shows the essential behavioral characteristics of sleep. Based on these analyses we next used immobility bouts of >5' as proxy for sleep in automatic activity monitoring records, and found that sleep is severely reduced in the presence of larvae that require feeding or pupae that are not fed. Reduced sleep was correlated with wax pot building, which is a behavior typical to nest founding mother queens. Sleep was also reduced in the presence of empty cocoons, but this effect was transient and reduced with time. This observation that is consistent with the presence of a sleep modulating pheromonal signal. These results provide the first evidence for brood modulation of sleep in an insect, and are consistent with the hypothesis that plasticity in sleep can evolve as a mechanism to improve care for dependent juveniles.

animal behavior and cognition↗