scholarly journals Inquiline social parasites as tools to unlock the secrets of insect sociality

2019 ◽  
Vol 374 (1769) ◽  
pp. 20180193 ◽  
Author(s):  
Alessandro Cini ◽  
Seirian Sumner ◽  
Rita Cervo
Keyword(s):  
Social Parasitism ◽  
Division Of Labour ◽  
Social Parasite ◽  
Social Parasites ◽  
Insect Societies ◽  
History Of ◽  
Reproductive Division Of Labour ◽  
Insect Sociality ◽  
Taxonomic Groups ◽  
Reproductive Division

Insect societies play a crucial role in the functioning of most ecosystems and have fascinated both scientists and the lay public for centuries. Despite the long history of study, we are still far from understanding how insect societies have evolved and how social cohesion in their colonies is maintained. Here we suggest inquiline social parasites of insect societies as an under-exploited experimental tool for understanding sociality. We draw on examples from obligate inquiline (permanent) social parasites in wasps, ants and bees to illustrate how these parasites may allow us to better understand societies and learn more about the evolution and functioning of insect societies. We highlight three main features of these social parasite–host systems—namely, close phylogenetic relationships, strong selective pressures arising from coevolution and multiple independent origins—that make inquiline social parasites particularly suited for this aim; we propose a conceptual comparative framework that considers trait losses, gains and modifications in social parasite–host systems. We give examples of how this framework can reveal the more elusive secrets of sociality by focusing on two cornerstones of sociality: communication and reproductive division of labour. Together with social parasites in other taxonomic groups, such as cuckoos in birds, social parasitism has a great potential to reveal the mechanisms and evolution of complex social groups. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

scholarly journals Adaptation and the genetics of social behaviour

2009 ◽  
Vol 364 (1533) ◽  
pp. 3209-3216 ◽  
Author(s):  
Laurent Keller
Keyword(s):  
Social Behaviour ◽  
Social Evolution ◽  
Division Of Labour ◽  
Chemical Signalling ◽  
Insect Societies ◽  
Genetic Mechanisms ◽  
Selective Forces ◽  
Group Members ◽  
Reproductive Division Of Labour ◽  
Reproductive Division

In recent years much progress has been made towards understanding the selective forces involved in the evolution of social behaviour including conflicts over reproduction among group members. Here, I argue that an important additional step necessary for advancing our understanding of the resolution of potential conflicts within insect societies is to consider the genetics of the behaviours involved. First, I discuss how epigenetic modifications of behaviour may affect conflict resolution within groups. Second, I review known natural polymorphisms of social organization to demonstrate that a lack of consideration of the genetic mechanisms involved may lead to erroneous explanations of the adaptive significance of behaviour. Third, I suggest that, on the basis of recent genetic studies of sexual conflict in Drosophila , it is necessary to reconsider the possibility of within-group manipulation by means of chemical substances (i.e. pheromones). Fourth, I address the issue of direct versus indirect genetic effects, which is of particular importance for the study of behaviour in social groups. Fifth, I discuss the issue of how a genetic influence on dominance hierarchies and reproductive division of labour can have secondary effects, for example in the evolution of promiscuity. Finally, because the same sets of genes (e.g. those implicated in chemical signalling and the responses that are triggered) may be used even in species as divergent as ants, cooperative breeding birds and primates, an integration of genetic mechanisms into the field of social evolution may also provide unifying ideas.

scholarly journals Honeybee Queen mandibular pheromone induces starvation in Drosophila melanogaster, implying a role for nutrition signalling in the evolution of eusociality.

2021 ◽  
Author(s):  
Mackenzie R Lovegrove ◽  
Elizabeth J Duncan ◽  
Peter K Dearden
Keyword(s):  
Drosophila Melanogaster ◽  
Division Of Labour ◽  
Starvation Response ◽  
Queen Mandibular Pheromone ◽  
Honeybee Queen ◽  
Insect Societies ◽  
Reproductive Division Of Labour ◽  
Evolution Of Eusociality ◽  
Reproductive Division ◽  
Behavioural Dominance

Eusocial insect societies are defined by the reproductive division of labour, a social structure that is generally enforced by the reproductive dominant or queen. Reproductive dominance is maintained through behavioural dominance in some species as well as production of queen pheromones in others, or a mixture of both. Queen mandibular pheromone (QMP) is produced by honeybee (Apis mellifera) queens and has been characterised chemically. How QMP acts to repress worker reproduction, and how it has evolved this activity, remains less well understood. Surprisingly, QMP is capable of repressing reproduction in non-target arthropods which have not co-evolved with QMP, are never exposed to QMP in nature, and are up to 530 million years diverged from the honeybee. Here we show that, in Drosophila melanogaster, QMP treatment mimics nutrient limiting conditions, leading to disrupted reproduction. Exposure to QMP induces an increase in food consumption, consistent with that observed in D. melanogaster in response to starvation conditions. This response induces the activation of two checkpoints within the ovary that inhibit oogenesis. The first is the 2a/b ovarian checkpoint in the germarium, which reduces the flow of presumptive oocytes. A stage 9 ovarian checkpoint is also activated, causing degradation of oocytes. The magnitude of activation of both checkpoints is indistinguishable between QMP treated and starved individuals. As QMP seems to trigger a starvation response in an insect highly diverged from honeybees, we propose that QMP originally evolved by co-opting nutrition signalling pathways to regulate reproduction, a key step in the evolution of eusociality.

scholarly journals Honeybees possess a structurally diverse and functionally redundant set of queen pheromones

2019 ◽  
Vol 286 (1905) ◽  
pp. 20190517 ◽  
Author(s):  
Sarah A. Princen ◽  
Ricardo Caliari Oliveira ◽  
Ulrich R. Ernst ◽  
Jocelyn G. Millar ◽  
Jelle S. van Zweden ◽  
...  
Keyword(s):  
Division Of Labour ◽  
Ovary Development ◽  
Mandibular Glands ◽  
Queen Mandibular Pheromone ◽  
Queen Pheromones ◽  
Honeybee Queen ◽  
Queen Signal ◽  
Insect Societies ◽  
Reproductive Division Of Labour ◽  
Reproductive Division

Queen pheromones, which signal the presence of a fertile queen and induce workers to remain sterile, play a key role in regulating reproductive division of labour in insect societies. In the honeybee, volatiles produced by the queen's mandibular glands have been argued to act as the primary sterility-inducing pheromones. This contrasts with evidence from other groups of social insects, where specific queen-characteristic hydrocarbons present on the cuticle act as conserved queen signals. This led us to hypothesize that honeybee queens might also employ cuticular pheromones to stop workers from reproducing. Here, we support this hypothesis with the results of bioassays with synthetic blends of queen-characteristic alkenes, esters and carboxylic acids. We show that all these compound classes suppress worker ovary development, and that one of the blends of esters that we used was as effective as the queen mandibular pheromone (QMP) mix. Furthermore, we demonstrate that the two main QMP compounds 9-ODA and 9-HDA tested individually were as effective as the blend of all four major QMP compounds, suggesting considerable signal redundancy. Possible adaptive reasons for the observed complexity of the honeybee queen signal mix are discussed.

scholarly journals Relatedness and the fraternal major transitions

2000 ◽  
Vol 355 (1403) ◽  
pp. 1647-1655 ◽  
Author(s):  
David C. Queller
Keyword(s):  
Kin Selection ◽  
Germ Line ◽  
Division Of Labour ◽  
Major Transitions ◽  
Insect Societies ◽  
Reproductive Division Of Labour ◽  
Special Relationships ◽  
Reproductive Division ◽  
Major Transitions In Evolution

Many of the major transitions in evolution involved the coalescence of independent lower–level units into a higher organismal level. This paper examines the role of kinship, focusing on the transitions to multicellularity in animals and to coloniality in insects. In both, kin selection based on high relatedness permitted cooperation and a reproductive division of labour. The higher relatedness of haplodiploid females to their sisters than to their offspring might not have been crucial in the origin of insect societies, and the transition to multicellularity shows that such special relationships are not required. When multicellular forms develop from a single cell, selfish conflict is minimal because each selfish mutant obtains only one generation of within–individual advantage in a chimaera. Conditionally expressed traits are particularly immune to within–individual selfishness because such mutations are rarely expressed in chimaeras. Such conditionally expressed altruism genes lead easily to the evolution of the soma, and the germ line might simply be what is left over. In most social insects, differences in relatedness ensure that there will be potential conflicts. Power asymmetries sometimes lead to such decisive settlements of conflicts that social insect colonies can be considered to be fully organismal.

scholarly journals Cooperative policing behaviour regulates reproductive division of labour in a termite

2020 ◽  
Vol 287 (1928) ◽  
pp. 20200780
Author(s):  
Qian Sun ◽  
Jordan D. Hampton ◽  
Austin Merchant ◽  
Kenneth F. Haynes ◽  
Xuguo Zhou
Keyword(s):  
Reproductive Potential ◽  
Reticulitermes Flavipes ◽  
Division Of Labour ◽  
Cooperative Effort ◽  
Insect Societies ◽  
Alarm Behaviour ◽  
Reproductive Division Of Labour ◽  
Eastern Subterranean Termite ◽  
Reproductive Conflicts ◽  
Reproductive Division

Reproductive conflicts are common in insect societies where helping castes retain reproductive potential. One of the mechanisms regulating these conflicts is policing, a coercive behaviour that reduces direct reproduction by other individuals. In eusocial Hymenoptera (ants, bees and wasps), workers or the queen act aggressively towards fertile workers, or destroy their eggs. In many termite species (order Blattodea), upon the death of the primary queen and king, workers and nymphs can differentiate into neotenic reproductives and inherit the breeding position. During this process, competition among neotenics is inevitable, but how this conflict is resolved remains unclear. Here, we report a policing behaviour that regulates reproductive division of labour in the eastern subterranean termite, Reticulitermes flavipes . Our results demonstrate that the policing behaviour is a cooperative effort performed sequentially by successful neotenics and workers. A neotenic reproductive initiates the attack of the fellow neotenic by biting and displays alarm behaviour. Workers are then recruited to cannibalize the injured neotenic. Furthermore, the initiation of policing is age-dependent, with older reproductives attacking younger ones, thereby inheriting the reproductive position. This study provides empirical evidence of policing behaviour in termites, which represents a convergent trait shared between eusocial Hymenoptera and Blattodea.

scholarly journals The evolution of social parasitism in Formica ants revealed by a global phylogeny

2020 ◽  
Author(s):  
Marek L Borowiec ◽  
Stefan P Cover ◽  
Christian Rabeling
Keyword(s):  
Life History ◽  
New World ◽  
Social Parasitism ◽  
Social Parasite ◽  
Colony Foundation ◽  
Parasite Diversity ◽  
Social Parasites ◽  
Evolutionary Trajectories ◽  
Competing Hypotheses ◽  
Temporary Social Parasitism

Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 178 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life-history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed the first global phylogeny of Formica ants and representative formicine outgroups. The genus Formica originated in the Old World during the Oligocene (~30 Ma ago) and dispersed multiple times to the New World. Within Formica, the capacity for dependent colony foundation and temporary social parasitism arose once from a facultatively polygynous, independently colony founding ancestor. Within this parasitic clade, dulotic social parasitism evolved once from a facultatively temporary parasitic ancestor that likely practiced colony budding frequently. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from different facultative parasitic backgrounds in socially polymorphic organisms. In contrast to inquiline ant species in other genera, the high social parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.

scholarly journals Conserved queen pheromones in bumblebees: A reply to Amsalem et al.

2016 ◽  
Author(s):  
Luke Holman ◽  
Jelle S van Zweden ◽  
Ricardo Caliari Oliveira ◽  
Annette van Oystaeyen ◽  
Tom Wenseleers
Keyword(s):  
Statistical Tests ◽  
Cuticular Hydrocarbon ◽  
Division Of Labour ◽  
Queen Pheromone ◽  
Worker Reproduction ◽  
Egg Laying ◽  
False Negatives ◽  
Evolutionarily Conserved ◽  
Reproductive Division Of Labour ◽  
Reproductive Division

In a recent study, Amsalem et al. performed experiments with Bombus impatiens bumblebees to test the hypothesis that saturated cuticular hydrocarbons are evolutionarily conserved signals used to regulate reproductive division of labour in many Hymenopteran social insects. They concluded that the cuticular hydrocarbon pentacosane (C25), previously identified as a queen pheromone in a congeneric bumblebee, does not affect worker reproduction in B. impatiens. Here we identify some significant shortcomings of Amsalem et al.’s study that make its conclusions unreliable. In particular, inappropriate statistical tests were used, and a reanalysis of their dataset found that C25 substantially reduced and delayed worker egg laying in B. impatiens. Additionally, the study’s low sample sizes (mean n per treatment = 13.6, range: 4-23) give it low power, not 99% power as claimed, meaning that some its non-significant results may be false negatives. Additionally, several confounding effects may have affected the results of both experimental manipulations in the study

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