scholarly journals Eusociality through conflict dissolution

2020 ◽  
Author(s):  
Mauricio González-Forero ◽  
Jorge Peña
Keyword(s):  
Worker Reproduction ◽  
Maternal Influence ◽  
Dissolution Mechanism ◽  
Evolutionary Transition ◽  
Evolutionary Time ◽  
Trade Off ◽  
Maternal Manipulation ◽  
Reproductive Division Of Labor ◽  
Reproductive Division ◽  
General Explanation

AbstractEusociality, where largely unreproductive offspring help their mothers reproduce, is a major form of social organization in social insects and other animals. An increasingly documented feature of eusociality is that mothers induce their offspring to help by means of hormones, pheromones, or behavioral displays, with evidence often indicating that offspring help voluntarily. The co-occurrence of widespread maternal influence and voluntary offspring help may be explained by what we call the converted helping hypothesis, whereby helping originally arising from maternal manipulation subsequently becomes voluntary. This hypothesis requires that parent-offspring conflict is eventually dissolved—for instance, if the benefit of helping increases sufficiently over evolutionary time. Here we show that maternal manipulation of offspring help enables the mother to increase her fertility to such extent that parent-offspring conflict is transformed into parent-offspring agreement. Such conflict dissolution mechanism requires that helpers alleviate the total percent life-history trade-off limiting maternal fertility, and results in reproductive division of labor, high queen fertility, and honest queen signaling suppressing worker reproduction, thus exceptionally recovering diverse features of eusociality. This mechanism is widely applicable, thus suggesting a general explanation for the origin of eusociality, the prevalence of maternal influence, and the offspring’s willingness to help. Overall, our results explain how a major evolutionary transition can happen from ancestral conflict.

scholarly journals Eusociality through conflict dissolution

2021 ◽  
Vol 288 (1949) ◽  
Author(s):  
Mauricio González-Forero ◽  
Jorge Peña
Keyword(s):  
Division Of Labour ◽  
Worker Reproduction ◽  
Maternal Influence ◽  
Dissolution Mechanism ◽  
Evolutionary Transition ◽  
Evolutionary Time ◽  
Trade Offs ◽  
Reproductive Division Of Labour ◽  
Reproductive Division ◽  
General Explanation

Eusociality, where largely unreproductive offspring help their mothers reproduce, is a major form of social organization. An increasingly documented feature of eusociality is that mothers induce their offspring to help by means of hormones, pheromones or behavioural displays, with evidence often indicating that offspring help voluntarily. The co-occurrence of maternal influence and offspring voluntary help may be explained by what we call the converted helping hypothesis, whereby maternally manipulated helping subsequently becomes voluntary. Such hypothesis requires that parent-offspring conflict is eventually dissolved—for instance, if the benefit of helping increases sufficiently over evolutionary time. We show that help provided by maternally manipulated offspring can enable the mother to sufficiently increase her fertility to transform parent-offspring conflict into parent-offspring agreement. This conflict-dissolution mechanism requires that helpers alleviate maternal life-history trade-offs, and results in reproductive division of labour, high queen fertility and honest queen signalling suppressing worker reproduction—thus exceptionally recovering diverse features of eusociality. As such trade-off alleviation seemingly holds widely across eusocial taxa, this mechanism offers a potentially general explanation for the origin of eusociality, the prevalence of maternal influence, and the offspring’s willingness to help. Overall, our results explain how a major evolutionary transition can happen from ancestral conflict.

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 Bumble bee queen pheromones are context-dependent

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Margarita Orlova ◽  
Etya Amsalem
Keyword(s):  
Social Context ◽  
Social Insects ◽  
Inhibitory Effect ◽  
Queen Pheromone ◽  
Worker Reproduction ◽  
Bumble Bee ◽  
Queen Pheromones ◽  
Visual Presence ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

AbstractQueen pheromones have long been studied as a major factor regulating reproductive division of labor in social insects. Hitherto, only a handful of queen pheromones were identified and their effects on workers have mostly been studied in isolation from the social context in which they operate. Our study examined the importance of behavioral and social context for the perception of queen semiochemicals by bumble bee workers. Our results indicate that a mature queen’s cuticular semiochemicals are capable of inhibiting worker reproduction only when accompanied by the queen’s visual presence and the offspring she produces, thus, when presented in realistic context. Queen’s chemistry, queen’s visual presence and presence of offspring all act to regulate worker reproduction, but none of these elements produces an inhibitory effect on its own. Our findings highlight the necessity to reconsider what constitutes a queen pheromone and suggest a new approach to the study of chemical ecology in social insects.

scholarly journals Bumble bee queen pheromones are context-dependent

2021 ◽  
Author(s):  
Margarita Orlova ◽  
Etya Amsalem
Keyword(s):  
Social Context ◽  
Social Insects ◽  
Inhibitory Effect ◽  
Queen Pheromone ◽  
Worker Reproduction ◽  
Bumble Bee ◽  
Queen Pheromones ◽  
Visual Presence ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

Abstract Queen pheromones have long been studied as a major factor regulating reproductive division of labor in social insects. Hitherto, only a handful of queen pheromones were identified and their effects on workers have mostly been studied in isolation from the social context in which they operate. Our study examined the importance of behavioral and social context for the perception of queen semiochemicals by bumble bee workers. Our results indicate that a mature queen’s semiochemicals are capable of inhibiting worker reproduction only when accompanied by the queen’s visual presence and the offspring she produces, thus, when presented in realistic context. Queen’s chemistry, queen’s visual presence and presence of offspring all act in synergy to regulate worker reproduction, but none of these elements produces an inhibitory effect on its own. Our findings highlight the necessity to reconsider what constitutes a queen pheromone and suggest a new approach to the study of chemical ecology in social insects.

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 Geometry shapes evolution of early multicellularity

2014 ◽  
Author(s):  
Eric Libby ◽  
Will Ratcliff ◽  
Mike Travisano ◽  
Ben Kerr
Keyword(s):  
Cell Death ◽  
Division Of Labor ◽  
Cell Number ◽  
Evolutionary Transition ◽  
Yeast Saccharomyces Cerevisiae ◽  
Evolutionary Transitions ◽  
Major Transitions ◽  
Reproductive Differentiation ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

Organisms have increased in complexity through a series of major evolutionary transitions, in which formerly autonomous entities become parts of a novel higher-level entity. One intriguing feature of the higher-level entity after some major transitions is a division of reproductive labor among its lower-level units. Although it can have clear benefits once established, it is unknown how such reproductive division of labor originates. We consider a recent evolution experiment on the yeast Saccharomyces cerevisiae as a unique platform to address the issue of reproductive differentiation during an evolutionary transition in individuality. In the experiment, independent yeast lineages evolved a multicellular “snowflake-like” cluster form in response to gravity selection. Shortly after the evolution of clusters, the yeast evolved higher rates of cell death. While cell death enables clusters to split apart and form new groups, it also reduces their performance in the face of gravity selection. To understand the selective value of increased cell death, we create a mathematical model of the cellular arrangement within snowflake yeast clusters. The model reveals that the mechanism of cell death and the geometry of the snowflake interact in complex, evolutionarily important ways. We find that the organization of snowflake yeast imposes powerful limitations on the available space for new cell growth. By dying more frequently, cells in clusters avoid encountering space limitations, and, paradoxically, reach higher numbers. In addition, selection for particular group sizes can explain the increased rate of apoptosis both in terms of total cell number and total numbers of collectives. Thus, by considering the geometry of a primitive multicellular organism we can gain insight into the initial emergence of reproductive division of labor during an evolutionary transition in individuality.

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 Chemical Variation among Castes, Female Life Stages and Populations of the Facultative Eusocial Sweat Bee Halictus rubicundus (Hymenoptera: Halictidae)

2021 ◽  
Author(s):  
Iris Steitz ◽  
Robert J Paxton ◽  
Stefan Schulz ◽  
Manfred Ayasse
Keyword(s):  
Chemical Communication ◽  
North American ◽  
Specific Chemical ◽  
Eusocial Insects ◽  
Queen Signal ◽  
Ovarian Activation ◽  
Chemical Profiles ◽  
Reproductive Division Of Labor ◽  
Reproductive Division ◽  
Eusocial Species

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.

scholarly journals Evolutionarily recent dual obligatory symbiosis among adelgids indicates a transition between fungus- and insect-associated lifestyles

2021 ◽  
Author(s):  
Gitta Szabó ◽  
Frederik Schulz ◽  
Alejandro Manzano-Marín ◽  
Elena Rebecca Toenshoff ◽  
Matthias Horn
Keyword(s):  
Defense Mechanisms ◽  
Amino Acid Production ◽  
Evolutionary Transition ◽  
Evolutionary Time ◽  
Evolutionary Trajectories ◽  
Host Infection ◽  
Phylogenomic Analyses ◽  
Time Specific ◽  
High Level ◽  
Metagenomic Approach

AbstractAdelgids (Insecta: Hemiptera: Adelgidae) form a small group of insects but harbor a surprisingly diverse set of bacteriocyte-associated endosymbionts, which suggest multiple replacement and acquisition of symbionts over evolutionary time. Specific pairs of symbionts have been associated with adelgid lineages specialized on different secondary host conifers. Using a metagenomic approach, we investigated the symbiosis of the Adelges laricis/Adelgestardus species complex containing betaproteobacterial (“Candidatus Vallotia tarda”) and gammaproteobacterial (“Candidatus Profftia tarda”) symbionts. Genomic characteristics and metabolic pathway reconstructions revealed that Vallotia and Profftia are evolutionary young endosymbionts, which complement each other’s role in essential amino acid production. Phylogenomic analyses and a high level of genomic synteny indicate an origin of the betaproteobacterial symbiont from endosymbionts of Rhizopus fungi. This evolutionary transition was accompanied with substantial loss of functions related to transcription regulation, secondary metabolite production, bacterial defense mechanisms, host infection, and manipulation. The transition from fungus to insect endosymbionts extends our current framework about evolutionary trajectories of host-associated microbes.

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