scholarly journals Regulatory Mechanisms Underlying the Differentiation of Neotenic Reproductives in Termites: Partial Release From Arrested Development

2021 ◽  
Vol 9 ◽  
Author(s):  
Kohei Oguchi ◽  
Kiyoto Maekawa ◽  
Toru Miura

Eusocial insects exhibit reproductive division of labor, in which only a part of colony members differentiates into reproductives. In termite colonies, the division of labors is performed among multiple types of individuals (i.e., castes), such as reproductives, workers, and soldiers to organize their society. Caste differentiation occurs according to extrinsic factors, such as social interactions, leading to developmental modifications during postembryonic development, and consequently, the caste ratio in a colony is appropriately coordinated. In particular, when the current reproductives die or become senescent, some immature individuals molt into supplementary reproductives, also known as “neotenics,” that take over the reproductive task in their natal colony. Neotenics exhibit variety of larval features, such as winglessness, and thus, immature individuals are suggested to differentiate by a partial release from arrested development, particularly in the reproductive organs. These neotenic features, which have long been assumed to develop via heterochronic regulation, provide us opportunities to understand the developmental mechanisms and evolutionary origin of the novel caste. This article overviews the accumulated data on the physiological and developmental mechanisms that regulate the neotenic differentiation in termites. Furthermore, the evolutionary trajectories leading to neotenic differentiation are discussed, namely the acquisition of a regulatory mechanism that enable the partial release from a developmentally arrested state.

Author(s):  
Iris Steitz ◽  
Robert J Paxton ◽  
Stefan Schulz ◽  
Manfred Ayasse

AbstractIn eusocial insects, chemical communication is crucial for mediating many aspects of social activities, especially the regulation of reproduction. Though queen signals are known to decrease ovarian activation of workers in highly eusocial species, little is known about their evolution. In contrast, some primitively eusocial species are thought to control worker reproduction through physical aggression by the queen rather than via pheromones, suggesting the evolutionary establishment of chemical signals with more derived sociality. However, studies supporting this hypothesis are largely missing. Socially polymorphic halictid bees, such as Halictus rubicundus, with social and solitary populations in both Europe and North America, offer excellent opportunities to illuminate the evolution of caste-specific signals. Here we compared the chemical profiles of social and solitary populations from both continents and tested whether (i) population or social level affect chemical dissimilarity and whether (ii) caste-specific patterns reflect a conserved queen signal. Our results demonstrate unique odor profiles of European and North American populations, mainly due to different isomers of n-alkenes and macrocyclic lactones; chemical differences may be indicative of phylogeographic drift in odor profiles. We also found common compounds overproduced in queens compared to workers in both populations, indicating a potential conserved queen signal. However, North American populations have a lower caste-specific chemical dissimilarity than European populations which raises the question if both use different mechanisms of regulating reproductive division of labor. Therefore, our study gives new insights into the evolution of eusocial behavior and the role of chemical communication in the inhibition of reproduction.


2020 ◽  
Author(s):  
Rachel A. Johnston ◽  
Philippe Vullioud ◽  
Jack Thorley ◽  
Henry Kirveslahti ◽  
Leyao Shen ◽  
...  

AbstractIn some mammals and many social insects, highly cooperative societies are characterized by reproductive division of labor, in which breeders and nonbreeders become behaviorally and morphologically distinct. While differences in behavior and growth between breeders and nonbreeders have been extensively described, little is known of their molecular underpinnings. Here, we investigate the consequences of breeding for skeletal morphology and gene regulation in highly cooperative Damaraland mole-rats. By experimentally assigning breeding ‘queen’ status versus nonbreeder status to age-matched littermates, we confirm that queens experience vertebral growth that likely confers advantages to fecundity. However, they also up-regulate bone resorption pathways and show reductions in femoral mass, which predicts increased vulnerability to fracture. Together, our results show that, as in eusocial insects, reproductive division of labor in mole-rats leads to gene regulatory rewiring and extensive morphological plasticity. However, in mole-rats, concentrated reproduction is also accompanied by costs to bone strength.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Rachel A Johnston ◽  
Philippe Vullioud ◽  
Jack Thorley ◽  
Henry Kirveslahti ◽  
Leyao Shen ◽  
...  

In some mammals and many social insects, highly cooperative societies are characterized by reproductive division of labor, in which breeders and nonbreeders become behaviorally and morphologically distinct. While differences in behavior and growth between breeders and nonbreeders have been extensively described, little is known of their molecular underpinnings. Here, we investigate the consequences of breeding for skeletal morphology and gene regulation in highly cooperative Damaraland mole-rats. By experimentally assigning breeding 'queen' status versus nonbreeder status to age-matched littermates, we confirm that queens experience vertebral growth that likely confers advantages to fecundity. However, they also up-regulate bone resorption pathways and show reductions in femoral mass, which predicts increased vulnerability to fracture. Together, our results show that, as in eusocial insects, reproductive division of labor in mole-rats leads to gene regulatory rewiring and extensive morphological plasticity. However, in mole-rats, concentrated reproduction is also accompanied by costs to bone strength.


1971 ◽  
Vol 19 (1) ◽  
pp. 85 ◽  
Author(s):  
RC Patel ◽  
JA Inamdar

Fourteen types of normal and abnormal stomatal structure and development in vegetative and floral organs of Physalis minima are presented. Those described include anomocytic, anisocytic, paracytic, and diacytic stomata, those transitional between paracytic and diacytic, and stomata with a single subsidiary cell. Anomalies observed are degeneration of the meristemoid, a persistent stomatal initial, single guard cells, twin stomata, single guard cells in relationship with a normal stoma, twin single guard cells, stomata with aborted guard cells, and arrested development. Development of the anomocytic type is haplocheilic or perigenous; that of the anisocytic, paracytic, diacytic, transitional, and with a single subsidiary cell is syndetocheilic or mesogenous. The persistent stomatal initials are variable in shape and occur solitary or in close relationship with the normal stoma. They may be notched and divide by centripetally extending furrows. Single guard cells develop directly from the meristemoid, or one of the guard cells degenerates before or after pore formation. Twin stomata, single guard cells in close relationship with normal stomata, and twin single guard cells develop from two adjacent meristemoids. Stomata with aborted guard cells are formed as a result of degeneration of guard cells. Arrested development results from early degeneration of nuclei and cytoplasm. The aberrent developments noticed here are partly due to extrinsic factors.


1988 ◽  
Vol 233 (1271) ◽  
pp. 175-189 ◽  

Primitively eusocial insects often lack morphological caste differentiation, leading to considerable flexibility in the social and reproductive roles that the adult insects may adopt. Although this flexibility and its consequences for social organization have received much attention there has been relatively little effort to detect any pre-imaginal effects leading to a bias in the potential caste of eclosing females. Experiments reported here show that only about 50 % of eclosing females of the tropical social wasp Ropalidia marginata build nests and lay eggs, in spite of being isolated from all conspecifics and being provided ad libitum food since eclosion. The number of empty cells in the parent nest, which we believe to be an indication of the queen’s declining influence, and a wasp’s own rate of feeding during adult life predict the probability of egg laying by eclosing females. These results call for an examination of the possibility that all females in primitively eusocial insect societies are not potentially capable of becoming egg layers and that reigning queens and possibly other adults exert an influence on the production of new queens.


Author(s):  
Rajani Sapkota ◽  
Cindy H. Nakatsu ◽  
Michael E. Scharf

Termites are eusocial insects that host a range of prokaryotic and eukaryotic gut symbionts and can differentiate into a range of caste phenotypes. Soldier caste differentiation from termite workers follows two successive molts (worker-presoldier-soldier) that are driven at the endocrine level by juvenile hormone (JH). While physiological and eusocial mechanisms tied to JH signaling have been studied, the role of gut symbionts in the caste differentiation process is poorly understood. Here, we used the JH analog-methoprene in combination with the antibiotic kanamycin to manipulate caste differentiation and gut bacterial loads in Reticulitermes flavipes termites via four bioassay treatments: kanamycin, methoprene, kanamycin+methoprene, and an untreated (negative) control. Bioassay results demonstrated a significantly higher number of presoldiers in the methoprene, highest mortality in kanamycin+methoprene, and significantly reduced protist numbers in all treatments except the untreated control. Bacterial 16S rRNA gene sequencing provided alpha and beta diversity results that mirrored bioassay findings. From ANCOM analysis, we found that several bacterial genera were differentially abundant among treatments. Finally, follow-up experiments showed that if methoprene and kanamycin or untreated termites are placed together, zero or rescued presoldier initiation (respectively) occurs. These findings reveal that endogenous JH selects for symbiont compositions required to successfully complete presoldier differentiation. However, if the gut is voided before the influx of JH, it cannot select for the necessary symbionts that are crucial for molting. Based on these results we are able to provide a novel example of linkages between gut microbial communities and host phenotypic plasticity.


BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Yi Bo Liu ◽  
Yao Yi ◽  
Amal Abdelmawla ◽  
Yun Lin Zheng ◽  
Zhi Jiang Zeng ◽  
...  

Abstract Background Nutrition and cell size play an important role in the determination of caste differentiation in queen and worker of honeybees (Apis mellifera), whereas the haploid genome dominates the differentiation of drones. However, the effects of female developmental environment on the development of males remain unclear. In this study, young drone larvae were transferred into worker cells (WCs) or remained in drone cells (DCs) to rear drones. The drone larvae were also grafted into queen cells (QCs) for 48 h and then transplanted into drone cells until emerging. Morphological indexes and reproductive organs of these three types of newly emerged drones were measured. Newly emerged drones and third instar drone larvae from WCs, DCs and QCs were sequenced by RNA sequencing (RNA-Seq). Results The amount of food remaining in cells of the QC and WC groups was significantly different to that in the DC group at the early larval stage. Morphological results showed that newly emerged DC drones had bigger body sizes and more well-developed reproductive tissues than WC and QC drones, whereas the reproductive tissues of QC drones were larger than those of WC drones. Additionally, whole body gene expression results showed a clear difference among three groups. At larval stage there were 889, 1761 and 1927 significantly differentially expressed genes (DEGs) in WC/DC, QC/DC and WC/QC comparisons, respectively. The number of DEGs decreased in adult drones of these three comparisons [678 (WC/DC), 338 (QC/DC) and 518 (WC/QC)]. A high number of DEGs were involved in sex differentiation, growth, olfaction, vision, mammalian target of rapamycin (mTOR), Wnt signaling pathways, and other processes. Conclusions This study demonstrated that the developmental environment of honeybee females can delay male development, which may serve as a model for understanding the regulation of sex differentiation and male development in social insects by environmental factors.


2020 ◽  
Author(s):  
Yi Bo Liu ◽  
Yao Yi ◽  
Amal Abdelmawla ◽  
Zhi Jiang Zeng ◽  
Xu Jiang He

Abstract Background Nutrition and cell size play an important role in the determination of caste differentiation in queen-worker of honeybee (Apis mellifera), whereas the haploid genome dominates the differentiation of drones. However, the effects of female developmental environment on the development of males remain unclear. In this study, young drone larvae were transferred into worker cells (WCs) or remained in drone cells (DCs) to rear drones. The parts of drone larvae were also grafted into queen cells (QCs) for 48 h and then transplanted into drone cells until emerging. Morphological indexes and reproductive organs of these three types of newly emerged drones were measured. Newly emerged drones and 3 d drone larvae from WCs, DCs and QCs were sequenced by RNA sequencing (RNA-Seq). Results Morphological results showed that newly emerged DC drones had bigger body sizes and more well-developed reproductive tissues than WC and QC drones, whereas the reproductive tissues of QC drones were relatively better than those of WC drones. Gene expression results showed a more clear difference among three groups. At the larval stage, there were 889, 1761 and 1927 significantly differentially expressed genes (DEGs) in WC/DC, QC/DC and WC/QC comparisons, respectively. The number of DEGs decreased in adult drones of these three comparisons [678 (WC/DC), 338 (QC/DC) and 518 (WC/QC)]. A high number of DEGs were involved in sex regulation, growth, olfaction, vision, mammalian target of rapamycin (mTOR), Wnt signaling pathways, etc. Weighted gene co-expression network analysis (WCGNA) showed that WC and DC larvae were closer than QC larvae, whereas QC and WC drones were closer than DC drones. These results revealed that DC drones had better development in the body and reproductive system than QC and WC drones. Conclusion This study demonstrated that the developmental environment of honeybee females including the larval diet and cell size delayed male development. Naturally, honeybee colony ovigerous workers in queen-less colonies or non-mated queens produce a large number of dysplasia drones which are not well-developed. Therefore, this study serves as a model for understanding the regulation of sexual differentiation in social insects by environmental factors.


2021 ◽  
Author(s):  
Marina N. Psalti ◽  
Dustin Gohlke ◽  
Romain Libbrecht

AbstractThe reproductive division of labor of eusocial insects, whereby one or several queens monopolize reproduction, evolved in a context of high genetic relatedness. However, many extant eusocial species have developed strategies that decrease genetic relatedness in their colonies, suggesting some benefits of the increased diversity. Multiple studies support this hypothesis by showing positive correlations between genetic diversity and colony fitness, as well as finding effects of experimental manipulations of diversity on colony performance. However, alternative explanations could account for most of these reports, and the benefits of diversity on fitness in eusocial insects still await validation. In this study, we experimentally increased worker diversity in the ant Lasius niger while controlling for typical confounding factors. We found that experimental colonies composed of workers coming from three different source colonies produced more larvae and showed more variation in size compared to groups of workers coming from a single colony. We propose that the benefits of increased diversity stemmed from an improved division of labor. Our study confirms that worker diversity enhances colony performance, thus providing a possible explanation for the evolution of multiply mated queens and multiple-queen colonies in many species of eusocial insects.


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