scholarly journals Identification of an ant queen pheromone regulating worker sterility

2010 ◽  
Vol 277 (1701) ◽  
pp. 3793-3800 ◽  
Author(s):  
Luke Holman ◽  
Charlotte G. Jørgensen ◽  
John Nielsen ◽  
Patrizia d'Ettorre
Keyword(s):  
Evolutionary Biology ◽  
Cuticular Hydrocarbon ◽  
Division Of Labour ◽  
Queen Pheromone ◽  
Lasius Niger ◽  
Strong Response ◽  
Selective Forces ◽  
The Right ◽  
Worker Sterility ◽  
Reproductive Division

The selective forces that shape and maintain eusocial societies are an enduring puzzle in evolutionary biology. Ordinarily sterile workers can usually reproduce given the right conditions, so the factors regulating reproductive division of labour may provide insight into why eusociality has persisted over evolutionary time. Queen-produced pheromones that affect worker reproduction have been implicated in diverse taxa, including ants, termites, wasps and possibly mole rats, but to date have only been definitively identified in the honeybee. Using the black garden ant Lasius niger , we isolate the first sterility-regulating ant queen pheromone. The pheromone is a cuticular hydrocarbon that comprises the majority of the chemical profile of queens and their eggs, and also affects worker behaviour, by reducing aggression towards objects bearing the pheromone. We further show that the pheromone elicits a strong response in worker antennae and that its production by queens is selectively reduced following an immune challenge. These results suggest that the pheromone has a central role in colony organization and support the hypothesis that worker sterility represents altruistic self-restraint in response to an honest quality signal.

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

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

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 Irreversible sterility of workers and high-volume egg production by queens in the stingless bee Tetragonula carbonaria

2020 ◽  
Vol 223 (18) ◽  
pp. jeb230599
Author(s):  
Francisco Garcia Bulle Bueno ◽  
Rosalyn Gloag ◽  
Tanya Latty ◽  
Isobel Ronai
Keyword(s):  
Social Insects ◽  
Egg Production ◽  
High Volume ◽  
Division Of Labour ◽  
Stingless Bee ◽  
Reproductive Capacity ◽  
The Social ◽  
Worker Sterility ◽  
Virgin Queens ◽  
Reproductive Division

ABSTRACTSocial insects are characterised by a reproductive division of labour between queens and workers. However, in the majority of social insect species, the workers are only facultatively sterile. The Australian stingless bee Tetragonula carbonaria is noteworthy as workers never lay eggs. Here, we describe the reproductive anatomy of T. carbonaria workers, virgin queens and mated queens. We then conduct the first experimental test of absolute worker sterility in the social insects. Using a controlled microcolony environment, we investigate whether the reproductive capacity of adult workers can be rescued by manipulating the workers' social environment and diet. The ovaries of T. carbonaria workers that are queenless and fed unrestricted, highly nutritious royal jelly remain non-functional, indicating they are irreversibly sterile and that ovary degeneration is fixed prior to adulthood. We suggest that T. carbonaria might have evolved absolute worker sterility because colonies are unlikely to ever be queenless.

scholarly journals Cheater genotypes in the parthenogenetic ant Pristomyrmex punctatus

2008 ◽  
Vol 276 (1656) ◽  
pp. 567-574 ◽  
Author(s):  
Shigeto Dobata ◽  
Tomonori Sasaki ◽  
Hideaki Mori ◽  
Eisuke Hasegawa ◽  
Masakazu Shimada ◽  
...  
Keyword(s):  
Evolutionary Biology ◽  
Division Of Labour ◽  
Evolution Of Cooperation ◽  
Phylogenetic Study ◽  
Population Genetic Analysis ◽  
Cooperative Tasks ◽  
History Of ◽  
Distinct Lineage ◽  
Pristomyrmex Punctatus ◽  
Reproductive Division

Cooperation is subject to cheating strategies that exploit the benefits of cooperation without paying the fair costs, and it has been a major goal of evolutionary biology to explain the origin and maintenance of cooperation against such cheaters. Here, we report that cheater genotypes indeed coexist in field colonies of a social insect, the parthenogenetic ant Pristomyrmex punctatus . The life history of this species is exceptional, in that there is no reproductive division of labour: all females fulfil both reproduction and cooperative tasks. Previous studies reported sporadic occurrence of larger individuals when compared with their nest-mates. These larger ants lay more eggs and hardly take part in cooperative tasks, resulting in lower fitness of the whole colony. Population genetic analysis showed that at least some of these large-bodied individuals form a genetically distinct lineage, isolated from cooperators by parthenogenesis. A phylogenetic study confirmed that this cheater lineage originated intraspecifically. Coexistence of cheaters and cooperators in this species provides a good model system to investigate the evolution of cooperation in nature.

scholarly journals The build-up of dominance hierarchies in eusocial insects

2022 ◽  
Vol 377 (1845) ◽  
Author(s):  
Hiroyuki Shimoji ◽  
Shigeto Dobata
Keyword(s):  
Division Of Labour ◽  
Pecking Order ◽  
Dominance Hierarchies ◽  
Eusocial Insects ◽  
Network Analyses ◽  
Current State ◽  
Individual Memory ◽  
Behavioural Interactions ◽  
Selective Forces ◽  
Reproductive Division

Reproductive division of labour is a hallmark of eusocial insects. However, its stability can often be hampered by the potential for reproduction by otherwise sterile nest-mates. Dominance hierarchy has a crucial role in some species in regulating which individuals reproduce. Compared with those in vertebrates, the dominance hierarchies in eusocial insects tend to involve many more individuals, and should require additional selective forces unique to them. Here, we provide an overview of a series of studies on dominance hierarchies in eusocial insects. Although reported from diverse eusocial taxa, dominance hierarchies have been extensively studied in paper wasps and ponerine ants. Starting from molecular physiological attributes of individuals, we describe how the emergence of dominance hierarchies can be understood as a kind of self-organizing process through individual memory and local behavioural interactions. The resulting global structures can be captured by using network analyses. Lastly, we argue the adaptive significance of dominance hierarchies from the standpoint of sterile subordinates. Kin selection, underpinned by relatedness between nest-mates, is key to the subordinates' acceptance of their positions in the hierarchies. This article is part of the theme issue ‘The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies’.

scholarly journals A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees ( Bombus impatiens )

2015 ◽  
Vol 282 (1817) ◽  
pp. 20151800 ◽  
Author(s):  
Etya Amsalem ◽  
Margarita Orlova ◽  
Christina M. Grozinger
Keyword(s):  
Bombus Terrestris ◽  
Division Of Labour ◽  
Queen Pheromone ◽  
Worker Reproduction ◽  
Egg Laying ◽  
Bombus Impatiens ◽  
Queen Pheromones ◽  
Reproductive Division Of Labour ◽  
Reproductive Division ◽  
Adult Exposure

The regulation of reproductive division of labour is a key component in the evolution of social insects. Chemical signals are important mechanisms to regulate worker reproduction, either as queen-produced pheromones that coercively inhibit worker reproduction or as queen signals that honestly advertise her fecundity. A recent study suggested that a conserved class of hydrocarbons serve as queen pheromones across three independent origins of eusociality. In bumblebees ( Bombus terrestris ), pentacosane ( C 25) was suggested to serve as a queen pheromone. Here, we repeat these studies using a different species of bumblebee ( Bombus impatiens ) with a more controlled experimental design. Instead of dequeened colonies, we used same-aged, three-worker queenless groups comprising either experienced or naive workers (with/without adult exposure to queen pheromone). We quantified three hydrocarbons ( C 23, C 25 and C 27) on the cuticular surfaces of females and tested their effects on the two worker types. Our results indicate differences in responses of naive and experienced workers, genetic effects on worker reproduction, and general effects of hydrocarbons and duration of egg laying on ovary resorption rates. However, we found no evidence to support the theory that a conserved class of hydrocarbons serve as queen pheromones or queen signals in Bombus impatiens .

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

PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3332 ◽  
Author(s):  
Luke Holman ◽  
Jelle S. van Zweden ◽  
Ricardo C. Oliveira ◽  
Annette van Oystaeyen ◽  
Tom Wenseleers
Keyword(s):  
Cuticular Hydrocarbons ◽  
Statistical Tests ◽  
Cuticular Hydrocarbon ◽  
Queen Pheromone ◽  
Egg Laying ◽  
False Negatives ◽  
Queen Pheromones ◽  
Evolutionarily Conserved ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

In a recent study, Amsalem, Orlova & Grozinger (2015) performed experiments withBombus impatiensbumblebees to test the hypothesis that saturated cuticular hydrocarbons are evolutionarily conserved signals used to regulate reproductive division of labor 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 inB. impatiens. Here we discuss some shortcomings of Amsalem et al.’s study that make its conclusions unreliable. In particular, several confounding effects may have affected the results of both experimental manipulations in the study. Additionally, the study’s low sample sizes (mean n per treatment = 13.6, range: 4–23) give it low power, not 96–99% power as claimed, such that its conclusions may be false negatives. Inappropriate statistical tests were also used, and our reanalysis found that C25substantially reduced and delayed worker egg laying inB. impatiens. We review the evidence that cuticular hydrocarbons act as queen pheromones, and offer some recommendations for future queen pheromone experiments.

scholarly journals Cryptic lineages hybridize for worker production in the harvester ant Messor barbarus

2016 ◽  
Vol 12 (11) ◽  
pp. 20160542 ◽  
Author(s):  
Victoria Norman ◽  
Hugo Darras ◽  
Christopher Tranter ◽  
Serge Aron ◽  
William O. H. Hughes
Keyword(s):  
Reproductive System ◽  
Division Of Labour ◽  
Insect Larvae ◽  
Messor Barbarus ◽  
Harvester Ant ◽  
Mitochondrial Data ◽  
Genetic Caste Determination ◽  
Worker Castes ◽  
Genetically Determined ◽  
Reproductive Division

The reproductive division of labour between queen and worker castes in social insects is a defining characteristic of eusociality and a classic example of phenotypic plasticity. Whether social insect larvae develop into queens or workers has long been thought to be determined by environmental cues, i.e. larvae are developmentally totipotent. Contrary to this paradigm, several recent studies have revealed that caste is determined by genotype in some ant species, but whether this is restricted to just a few exceptional species is still unclear. Here, we show that the Mediterranean harvester ant Messor barbarus possesses an unusual reproductive system, in which the female castes are genetically determined. Using both nuclear and mitochondrial data, we show that Iberian populations have two distinct, cryptic lineages. Workers are always inter-lineage hybrids whereas queens are always produced from pure-lineage matings. The results suggest that genetic caste determination may be more widespread in ants than previously thought, and that further investigation in other species is needed to understand the frequency and evolution of this remarkable reproductive system.

scholarly journals Major Evolutionary Transitions in Social Insects, the Importance of Worker Sterility and Life History Trade-Offs

2021 ◽  
Vol 9 ◽  
Author(s):  
Abel Bernadou ◽  
Boris H. Kramer ◽  
Judith Korb
Keyword(s):  
Life History ◽  
Social Insects ◽  
Division Of Labour ◽  
Evolutionary Transitions ◽  
Individual Level ◽  
Individual Fitness ◽  
Trade Offs ◽  
Group Members ◽  
The Individual ◽  
Worker Sterility

The evolution of eusociality in social insects, such as termites, ants, and some bees and wasps, has been regarded as a major evolutionary transition (MET). Yet, there is some debate whether all species qualify. Here, we argue that worker sterility is a decisive criterion to determine whether species have passed a MET (= superorganisms), or not. When workers are sterile, reproductive interests align among group members as individual fitness is transferred to the colony level. Division of labour among cooperating units is a major driver that favours the evolution of METs across all biological scales. Many METs are characterised by a differentiation into reproductive versus maintenance functions. In social insects, the queen specialises on reproduction while workers take over maintenance functions such as food provisioning. Such division of labour allows specialisation and it reshapes life history trade-offs among cooperating units. For instance, individuals within colonies of social insects can overcome the omnipresent fecundity/longevity trade-off, which limits reproductive success in organisms, when increased fecundity shortens lifespan. Social insect queens (particularly in superorganismal species) can reach adult lifespans of several decades and are among the most fecund terrestrial animals. The resulting enormous reproductive output may contribute to explain why some genera of social insects became so successful. Indeed, superorganismal ant lineages have more species than those that have not passed a MET. We conclude that the release from life history constraints at the individual level is a important, yet understudied, factor across METs to explain their evolutionary success.

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