scholarly journals The Doublesex sex determination pathway regulates reproductive division of labor in honey bees

2018 ◽  
Author(s):  
Mariana Velasque ◽  
Lijun Qiu ◽  
Alexander S. Mikheyev
Keyword(s):  
Division Of Labor ◽  
Honey Bees ◽  
Regulatory Network ◽  
Worker Reproduction ◽  
Ovary Development ◽  
Secondary Sexual Characteristics ◽  
Sexual Characteristics ◽  
Fertility Signalling ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

AbstractEusociality, the ultimate level of social organization, requires reproductive division of labor, and a sophisticated system of communication to maintain societal homeostasis. Reproductive division of labor is maintained by physiological differences between reproductive and sterile castes, typically dictated by pheromonal queen fertility signals that suppress worker reproduction. Intriguingly, reproduction and pheromonal signalling share regulatory machinery across insects.The gene Doublesex (Dsx) controls somatic sex determination and differentiation, including the development of ovaries and secondary sexual characteristics, such as pheromonal signalling. We hypothesized that this regulatory network was co-opted during eusocial evolution to regulate reproductive division of labor. Taking advantage of the breakdown in reproductive division of labor that occurs in honey bees when workers commence to lay eggs in the absence of a queen, we knocked down Dsx to observe effects on ovary development and fertility signal production. As expected, treated workers had lower levels of egg yolk protein, for which Dsx is a cis-regulatory enhancer in other insects, and greatly reduced ovary development. Also as expected, while control workers increased their levels of pheromonal fertility signals, treated workers did not, confirming the role of Dsx in regulating pheromone biosynthesis. We further found that Dsx is part of a large network enriched for regulatory proteins, which is also involved during early larval development, and upregulated in queen-destined larvae. Thus, the ancient developmental framework controlling sex specification and reproduction in solitary insects has been exapted for eusociality, forming the basis for reproductive division of labor and pheromonal signalling pathways.Significance statementComplex social insect societies rely on division of reproductive labor among their members. Reproductive individuals (‘queens’) suppress ‘worker’ reproduction using pheromonal fertility signalling. We show that an ancient regulatory network that controls specification of sex and secondary sexual characteristics in solitary insects, has been co-opted for both both pheromonal signalling and ovary inactivation in honey bees. In addition, this network is also active during caste specification that takes place during the first few days of larval life. These results show that pheromonal signalling and ovary development share a common regulatory framework, potentially explaining why fertility signalling is ‘honest.’ Furthermore, they show that higher levels of biological complexity can arise by rewiring and elaborating ancestral gene regulatory networks.

scholarly journals A small family business: synergistic and additive effects of the queen and the brood on worker reproduction in a primitively eusocial bee

2019 ◽  
Author(s):  
Margarita Orlova ◽  
Jesse Starkey ◽  
Etya Amsalem
Keyword(s):  
Division Of Labor ◽  
Worker Reproduction ◽  
Egg Laying ◽  
Brain Gene Expression ◽  
Worker Behavior ◽  
Social Species ◽  
Eusocial Bees ◽  
Reproductive Division Of Labor ◽  
Reproductive Division ◽  
Primitively Eusocial

AbstractThe mechanisms that maintain reproductive division of labor in social insects are still incompletely understood. Most studies focus on the relationship between adults, overlooking another important stakeholder in the game – the juvenile offspring. Recent studies from various social species show that not only the queen, but also the brood regulates reproductive division of labor between females, but how the two coordinate to maintain reproductive monopoly remained unexplored.Our study aims at disentangling the roles of the brood and the queen in regulating worker reproduction in primitively eusocial bees. We examined the effects induced by the brood and queen, separately and together, on the behavioral, physiological and brain gene expression of Bombus impatiens workers. We found that young larvae induce a releaser effect in workers, decreasing egg laying and aggressive behaviors, while the queen induces both releaser and primer effects, modifying worker aggressive and egg laying behavior and reproductive physiology. The expression of reproduction- and aggression-related genes was altered in the presence of both queen and brood, but the effect was stronger or the same in the presence of the queen.We identified two types of interactions between the queen and the brood in regulating worker reproduction: (1) synergistic interactions regulating worker physiology, where the combined effect of the queen and the brood was greater than each of them separately; (2) additive interactions regulating worker behavior, where the combined effects of the queen and the brood are the gross sum of their separated effects. In these interactions the brood acted in a manner similar to the queen but to a much smaller extent and improved the quality of the effect induced by the queen. Our results suggest that the queen and the brood of primitively eusocial bees coordinate synergistically, additively, and sometimes even redundantly to regulate worker behavior and reproduction, and the interaction between them exists in multiple regulatory levels.

scholarly journals Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity

2020 ◽  
Author(s):  
Rachel A. Johnston ◽  
Philippe Vullioud ◽  
Jack Thorley ◽  
Henry Kirveslahti ◽  
Leyao Shen ◽  
...  
Keyword(s):  
Division Of Labor ◽  
Morphological Plasticity ◽  
Skeletal Morphology ◽  
Eusocial Insects ◽  
Mole Rat ◽  
Gene Regulatory ◽  
Reproductive Division Of Labor ◽  
Reproductive Division ◽  
Skeletal Integrity ◽  
Vertebral Growth

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.

scholarly journals Morphological and genomic shifts in mole-rat 'queens' increase fecundity but reduce skeletal integrity

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Rachel A Johnston ◽  
Philippe Vullioud ◽  
Jack Thorley ◽  
Henry Kirveslahti ◽  
Leyao Shen ◽  
...  
Keyword(s):  
Division Of Labor ◽  
Morphological Plasticity ◽  
Skeletal Morphology ◽  
Eusocial Insects ◽  
Mole Rat ◽  
Gene Regulatory ◽  
Reproductive Division Of Labor ◽  
Reproductive Division ◽  
Skeletal Integrity ◽  
Vertebral Growth

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.

scholarly journals Reproductive constraint is a developmental mechanism that maintains social harmony in advanced ant societies

2008 ◽  
Vol 105 (46) ◽  
pp. 17884-17889 ◽  
Author(s):  
Abderrahman Khila ◽  
Ehab Abouheif
Keyword(s):  
Molecular Mechanisms ◽  
Worker Reproduction ◽  
Developmental Genetic ◽  
Potential Conflict ◽  
Trophic Eggs ◽  
Maternal Determinants ◽  
Colony Efficiency ◽  
Reproductive Division Of Labor ◽  
Reproductive Division ◽  
Colony Level

A hallmark of eusociality in ants is the reproductive division of labor between queens and workers. Yet, nothing is known about the molecular mechanisms underlying reproduction in this group. We therefore compared the developmental genetic capacity of queens and workers to reproduce in several eusocially advanced species from the two largest subfamilies of ants, the Myrmicinae and Formicinae. In flies, the asymmetric localization of maternally encoded determinants (mRNAs and proteins) during oogenesis establishes oocyte polarity and subsequently ensures proper embryonic development. Vasa and nanos, two key maternal determinants, are properly localized in the posterior of queen oocytes, but their localization is impaired in those of the workers. This mislocalization leads to severe embryonic defects in worker progeny, and therefore, represents a constraint on worker reproduction that we call ‘reproductive constraint.’ We show that reproductive constraint is phylogenetically widespread, and is at high levels in most species tested. Reproductive constraint can simultaneously reduce or eliminate the workers' ability to produce viable eggs for reproduction, while preserving their ability to produce trophic eggs for nutrition, and thus, may have been the basis for the evolutionary retention of worker ovaries in the majority of ants. We propose that high levels of reproductive constraint has most likely evolved as a consequence of selection at the colony level to reduce or eliminate any potential conflict over worker reproduction, therefore maintaining harmony and colony efficiency in advanced ant societies.

scholarly journals Topological constraints in early multicellularity favor reproductive division of labor

2019 ◽  
Author(s):  
David Yanni ◽  
Shane Jacobeen ◽  
Pedro Márquez-Zacarías ◽  
Joshua S Weitz ◽  
William C. Ratcliff ◽  
...  
Keyword(s):  
Division Of Labor ◽  
Resource Sharing ◽  
Evolutionary Biology ◽  
Large Body ◽  
Concave Function ◽  
Cellular Interactions ◽  
Wide Range ◽  
Classical Models ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

Reproductive division of labor (e.g., germ-soma specialization) is a hallmark of the evolution of multicellularity, signifying the emergence of a new type of individual and facilitating the evolution of increased organismal complexity. A large body of work from evolutionary biology, economics, and ecology has shown that specialization is beneficial when further division of labor produces an accelerating increase in absolute productivity (i.e., productivity is a convex function of specialization). Here we show that reproductive specialization is qualitatively different from classical models of resource sharing, and can evolve even when the benefits of specialization are saturating (i.e., productivity is a concave function of specialization). Through analytical theory and evolutionary individual based simulations, our work demonstrates that reproductive specialization is strongly favored in sparse networks of cellular interactions, such as trees and filaments, that reflect the morphology of early, simple multicellular organisms, highlighting the importance of restricted social interactions in the evolution of reproductive specialization. More broadly, we find that specialization is strongly favored, despite saturating returns on investment, in a wide range of scenarios in which sharing is asymmetric.

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