scholarly journals Suppressed eusocial reproduction supports evolutionary convergence over co-option

2021 ◽  
Author(s):  
Mariana Velasque ◽  
Tan Yongkai ◽  
Andrew W Liu ◽  
Nicholas M Luscombe ◽  
Jai A Denton

Eusocial insects are characterized by the presence of division of labour between reproductive (i.e. workers) and non-reproductive (i.e. queens) individuals. In eusocial insects, such as wasps, ants, honeybees and termites, such reproductive division of labour is mediated by the use of unique pheromones. In eusocial animals, pheromones control two distinct aspects of the division of labour: reproduction and division of tasks amongst workers. It has been suggested that eusociality arose independently on several occasions from pheromone-mediated co-option of pathways regulating the reproductive life cycle of solitary insects. Transcriptomic analysis has supported the co-option of similar pathways in each independently evolved eusocial insect. Using a solitary insect model, we sought to determine if these similar transcriptomic signals resulted from the co-option of similar pathways or varying pathways subject to convergent evolution. We measured the transcriptomic and physiological response of Drosophila melanogaster to pheromones from bumblebees, honey bees, and termites. In each case we observed a strong physiological response - the reduction of ovary size. However, employing conventional differential gene expression analysis and several forms of network analysis, we were unable to detect any conserved pathway or genes acting as a primer for eusociality. This strongly suggests that pheromone-mediated eusociality is the result of convergent evolution. Wherein a physiological response, such as reduced reproductive capacity, acts as the primer for eusociality and is subsequently refined.

2020 ◽  
Vol 64 (4-5-6) ◽  
pp. 267-273
Author(s):  
Sruthi Unnikrishnan ◽  
Raghavendra Gadagkar

Division of labour among workers (non-reproductive division of labour), a characteristic feature of eusocial insects enables the efficient functioning of their colonies. In many advanced insect societies division of labour is based on age (age polyethism). Primitively eusocial insects however are believed to have a weak age polyethism. Here we investigated the role of age in non-reproductive division of labour in the tropical primitively eusocial wasp, Ropalidia cyathiformis and compared it with that in Ropalidia marginata, a congeneric species that exhibits relatively strong age polyethism. Age had a significant effect on the first performance of the four tasks studied; tasks were initiated in the sequence feed larva, build, bring food and bring building material. We measured task performance as the absolute frequency of tasks performed (FTP) and the probability of performing a task relative to other tasks (PTP) and age as absolute age in days since eclosion as well as relative age compared to nestmates. FTP varied significantly with both absolute and relative age, although absolute age explained more variance. PTP varied significantly with absolute age but not always with relative age. This is contrary to R. marginata, where more variation is explained by relative age than by absolute age. There was no trade-off between intranidal and extranidal tasks in R. cyathiformis unlike in R. marginata where the frequency of intranidal tasks decreased and that of extranidal tasks increased with age. We conclude that age polyethism is weak and less flexible in R. cyathiformis compared to that in R. marginata.


2015 ◽  
Vol 93 (8) ◽  
pp. 615-625 ◽  
Author(s):  
M.H. Richards ◽  
C. Course

Reproductive division of labour in social carpenter bees differs from that in classically eusocial insects because reproductive output and ergonomic inputs are positively correlated—dominant females monopolize both foraging and reproduction. We quantified ergonomic skew in the facultatively social bee Xylocopa virginica (L., 1771) (eastern carpenter bee) based on detailed observations of foraging activity by individually marked females in 2009. Unusually for a univoltine bee, this species exhibits a spring foraging phase during which females feed pollen to other adults, probably as part of behavioural interactions to establish dominance hierarchies. During brood-provisioning, foraging in social nests was dominated by one female at a time, with replacement by a succession of foragers as dominants disappeared and were succeeded by a subordinate. The principal foragers (individuals that did the largest share of foraging in each colony) did 85%–100% of all pollen trips, so contributions to pollen-provisioning by female nest mates were highly uneven. Individual foraging rate was unaffected by group size and total colony foraging effort was a function of the number of foragers per group. Transient females that moved to new nests were as successful in achieving dominant forager status as females resident in their natal nests. This evidence indicates that colony social organisation is based on reproductive queues, whereby the first-ranked bee is the dominant forager and subordinates queue for opportunities to replace her.


2014 ◽  
Vol 281 (1793) ◽  
pp. 20141411 ◽  
Author(s):  
Henry Ferguson-Gow ◽  
Seirian Sumner ◽  
Andrew F. G. Bourke ◽  
Kate E. Jones

Division of labour is central to the ecological success of eusocial insects, yet the evolutionary factors driving increases in complexity in division of labour are little known. The size–complexity hypothesis proposes that, as larger colonies evolve, both non-reproductive and reproductive division of labour become more complex as workers and queens act to maximize inclusive fitness. Using a statistically robust phylogenetic comparative analysis of social and environmental traits of species within the ant tribe Attini, we show that colony size is positively related to both non-reproductive (worker size variation) and reproductive (queen–worker dimorphism) division of labour. The results also suggested that colony size acts on non-reproductive and reproductive division of labour in different ways. Environmental factors, including measures of variation in temperature and precipitation, had no significant effects on any division of labour measure or colony size. Overall, these results support the size–complexity hypothesis for the evolution of social complexity and division of labour in eusocial insects. Determining the evolutionary drivers of colony size may help contribute to our understanding of the evolution of social complexity.


2016 ◽  
Author(s):  
Luke Holman ◽  
Jelle S van Zweden ◽  
Ricardo Caliari Oliveira ◽  
Annette van Oystaeyen ◽  
Tom Wenseleers

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


2009 ◽  
Vol 364 (1533) ◽  
pp. 3209-3216 ◽  
Author(s):  
Laurent Keller

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.


2021 ◽  
Author(s):  
Guy Cooper ◽  
Hadleigh Frost ◽  
Ming Liu ◽  
Stuart West

Recent theory has overturned the assumption that accelerating returns from individual specialisation are required to favour the evolution of division of labour. Yanni et al. (2020) showed that topologically constrained groups, where cells cooperate with only direct neighbours such as for filaments or branching growths, can evolve a reproductive division of labour even with diminishing returns from individual specialisation. We developed a conceptual framework and specific models to investigate the factors that can favour the initial evolution of reproductive division of labour. We found that selection for division of labour in topologically constrained groups: (1) is not a single mechanism to favour division of labour – depending upon details of the group structure, division of labour can be favoured for different reasons; (2) always involves an efficiency benefit at the level of group fitness; and (3) requires a mechanism of coordination to determine which individuals perform which tasks. Given that such coordination is unlikely to evolve before division of labour, this limits the extent to which topological constraints could have favoured the initial evolution of division of labour. We conclude by suggesting experimental designs that could determine why division of labour is favoured in the natural world.


2021 ◽  
Author(s):  
Mackenzie R Lovegrove ◽  
Elizabeth J Duncan ◽  
Peter K Dearden

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.


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