Hybridization enables the fixation of selfish queen genotypes in eusocial colonies.
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ABSTRACT:
SUBMITTER: Weyna A
PROVIDER: S-EPMC8645202 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Eusocial insects are crucial to many ecosystems, and particularly the honeybee (Apis mellifera). One approach to facilitate their study in molecular genetics, is to consider whole-colony genotyping by combining DNA of multiple individuals in a single pool sequencing experiment. Cheap and fast, this technique comes with the drawback of producing data requiring dedicated methods to be fully exploited. Despite this limitation, pool sequencing data have been shown to be informative and cost-effective when working on random mating populations. Here, we present new statistical methods for exploiting pool sequencing of eusocial colonies in order to reconstruct the genotypes of the queen of such colony. This leverages the possibility to monitor genetic diversity, perform genomic-based studies or implement selective breeding. Using simulations and honeybee real data, we show that the new methods allow for a fast and accurate estimation of the queen's genetic ancestry, with correlations of about 0.9 to that obtained from individual genotyping. Also, it allows for an accurate reconstruction of the queen genotypes, with about 2% genotyping error. We further validate these inferences using experimental data on colonies with both pool sequencing and individual genotyping of drones. In brief, in this study we present statistical models to accurately estimate the genetic ancestry and reconstruct the genotypes of the queen from pool sequencing data from workers of an eusocial colony. Such information allows to exploit pool sequencing for traditional population genetics analyses, association studies and for selective breeding. While validated in Apis mellifera, these methods are applicable to other eusocial hymenopterans.
| S-EPMC9796407 | biostudies-literature
Project description:Colonies of insects such as ants and honeybees are commonly viewed as 'superorganisms', with division of labour between reproductive 'germline-like' queens and males and 'somatic' workers. On this view, properties of the superorganismal colony are comparable with those of solitary organisms to such an extent that the colony itself can be viewed as a unit analogous to an organism. Thus, the concept of a superorganism can be useful as a guide to thinking about life history and allocation traits of colonies as a whole. A pattern that seems to reoccur in insects with superorganismal societies is size dimorphism between queens and males, where queens tend to be larger than males. It has been proposed that this is analogous to the phenomenon of anisogamy at the level of gametes in organisms with separate sexes; more specifically, it is suggested that this caste dimorphism may have evolved via similar selection pressures as gamete dimorphism arises in the 'gamete competition' theory for the evolution of anisogamy. In this analogy, queens are analogous to female gametes, males are analogous to male gametes, and colony survival is analogous to zygote survival in gamete competition theory. Here, we explore if this question can be taken beyond an analogy, and whether a mathematical model at the superorganism level, analogous to gamete competition at the organism level, may explain the caste dimorphism seen in superorganismal insects. We find that the central theoretical idea holds, but that there are also significant differences between the way this generalized 'propagule competition' theory operates at the levels of solitary organisms and superorganisms. In particular, we find that the theory can explain superorganismal caste dimorphism, but compared with anisogamy evolution, a central coevolutionary link is broken, making the requirements for the theory to work less stringent than those found for the evolution of anisogamy.
| S-EPMC7341914 | biostudies-literature
Project description:In insect societies, both queens and workers produce chemicals that reliably signal caste membership and reproductive status. The mechanisms that help to maintain the honesty of such queen and fertility signals, however, remain poorly studied. Here we test if queen signal honesty could be based on the shared endocrine control of queen fertility and the production of specific signals. In support of this "hormonal pleiotropy" hypothesis, we find that in the common wasp, application of methoprene (a juveline hormone analogue) caused workers to acquire a queen-like cuticular hydrocarbon profile, resulting in the overproduction of known queen pheromones as well as some compounds typically linked to worker fertility. By contrast, administration of precocene-I (a JH inhibitor) had a tendency to have the opposite effect. Furthermore, a clear gonadotropic effect of JH in queens was suggested by the fact that circulating levels of JH were ca. 2 orders of magnitude higher in queens than those in workers and virgin, non-egg-laying queens, even if methoprene or precocene treatment did not affect the ovary development of workers. Overall, these results suggest that queen signal honesty in this system is maintained by queen fertility and queen signal production being under shared endocrine control.
| S-EPMC5431770 | biostudies-literature
Project description:Models of sex-allocation conflict are central to evolutionary biology but have mostly assumed static decisions, where resource allocation strategies are constant over colony lifespan. Here, we develop a model to study how the evolution of dynamic resource allocation strategies is affected by the queen-worker conflict in annual eusocial insects. We demonstrate that the time of dispersal of sexuals affects the sex-allocation ratio through sexual selection on males. Furthermore, our model provides three predictions that depart from established results of classic static allocation models. First, we find that the queen wins the sex-allocation conflict, while the workers determine the maximum colony size and colony productivity. Second, male-biased sex allocation and protandry evolve if sexuals disperse directly after eclosion. Third, when workers are more related to new queens, then the proportional investment into queens is expected to be lower, which results from the interacting effect of sexual selection (selecting for protandry) and sex-allocation conflict (selecting for earlier switch to producing sexuals). Overall, we find that colony ontogeny crucially affects the outcome of sex-allocation conflict because of the evolution of distinct colony growth phases, which decouples how queens and workers affect allocation decisions and can result in asymmetric control.
| S-EPMC6593813 | biostudies-literature
Project description:Queen signals are known to regulate reproductive harmony within eusocial colonies by influencing worker behavior and ovarian physiology. However, decades of research have resulted in the identification of just a few queen signals, and studies of their mode of action are rare. Our aim was to identify queen recognition signals in the halictid bee Lasioglossum pauxillum and to analyze caste differences in the olfactory perception of queen signals in L. pauxillum and the closely related species L. malachurum. We performed chemical analyses and bioassays to test for caste differences in chemical profiles and worker behavior influenced by queen-specific compounds in L. pauxillum. Our results indicated that caste differences in the chemical profiles were mainly attributable to higher amounts of macrocyclic lactones in queens. Bioassays demonstrated a higher frequency of subordinate behavior in workers elicited by queen-specific amounts of macrocyclic lactones. Thus, macrocyclic lactones function as queen recognition signals in L. pauxillum, as in L. malachurum. Using electrophysiological analyses, we have demonstrated that queens of both tested species lack antennal reactions to certain macrocyclic lactones. Therefore, we assume that this is a mechanism to prevent reproductive self-inhibition in queens. Our results should stimulate debate on the conservation and mode of action of queen signals.
| S-EPMC6955767 | biostudies-literature
Project description:Insect eusociality is characterized by cooperative brood care, reproductive division of labour and multiple generations of adults within a colony. The morphological specializations of the different termite castes from Burmese amber were recently reported, indicating the termites possessed advanced sociality in the mid-Cretaceous. Unfortunately, all the reported Cretaceous termites are individually preserved, which does not cover the behaviours of the cooperative brood care and multiple generations of adults in the nests of the Cretaceous termites. Herein, we report three eusocial aggregations from colonies of the oldest known Stolotermitidae, Cosmotermes gen. nov., in 100 Ma mid-Cretaceous Burmese amber. One large aggregation, comprising 8 soldiers, 56 workers/pseudergates and 25 immatures of different instars, additionally presents the behaviours of cooperative brood care and overlapping generations. Furthermore, taphonomic evidence indicates Cosmotermes most probably dwelled in damp/rotting wood, which provides a broader horizon of the early societies and ecology of the eusocial Cosmotermes.
| S-EPMC8288961 | biostudies-literature
Project description:Invasive social insects rank among the most damaging of terrestrial species. They are responsible for extensive damage and severely threaten the biodiversity of environments where they are introduced. Variation in colony social form commonly occurs in introduced populations of yellowjacket wasps (genus Vespula). In particular, invasive colonies may contain multiple queens (i.e., polygyne) and persist several years, while in the native range, the colonies are usually annual and harbor a single queen (i.e., monogyne). In this study, we used genome-wide loci obtained by double digest restriction site-associated DNA sequencing (RADseq) to investigate the genetic structure and queen turnover in colonies of the western yellowjacket, Vespula pensylvanica, in their introduced range in Hawaii. Of the 27 colonies monitored over four months (October-January), 19 were polygyne and already contained multiple queens on the first day of sampling. Contrary to previous speculation, this finding suggests that polygyny often arises early in the annual colony cycle, before the production of new queens in the fall. Furthermore, polygyne colonies exhibited a prolonged average lifespan relative to those headed by a single queen. As a result, there is no clear window during which colony eradication efforts would be more effective than upon first discovery. The relatedness among nestmate queens was slightly above zero, indicating that these colonies are generally composed of nonrelatives. The queen turnover within each colony was low, and we detected some full-sibling workers sampled up to four months apart. Finally, we did not detect any population structure among colonies, suggesting that queens disperse up to several kilometers. Taken together, our results provide the first insights into the requeening dynamics in this invasive and incipiently polygyne population and illuminate the early establishment of multiple long-lasting queens in these damaging colonies.
| S-EPMC8674895 | biostudies-literature
Project description:We investigated how group members achieve collective decision-making, by considering individual intrinsic behavioural rules and behavioural mechanisms for maintaining social integration. Using a simulated burrow environment, we investigated the behavioural rules of coordinated workload for soil distribution in a eusocial mammal, the naked mole-rat (Heterocephalus glaber). We tested two predictions regarding a distinct role of the queen, a socially dominant individual in the caste system: the presence of a queen would increase the workload of other caste individuals, and the cues by a queen would affect the soil distribution. In experiment 1, we placed four individuals of various castes from the same colony into an experimental burrow. Workers exhibited the highest frequency of workload compared to other castes. The presence of a queen activated the workload by other individuals. Individuals showed a consistent workload in a particular direction so as to bias the soil distribution. These results suggest that individuals have a consensus on soil distribution and that the queen plays a distinct role. In experiment 2, we placed the odour of a queen in one of four cells and observed its effect on other individuals' workload and soil distribution. Relative to other cells, individuals frequently dug in the queen cell so the amount of soil in the queen cell decreased. These results suggest that queen odour is an important cue in coordinated workload and soil distribution in this species.
| S-EPMC3434143 | biostudies-literature
Project description:This experiment was designed to identify gene expression differences in young bees raised in colonies with a queen, with queen mandibular pheromone (QMP), or without a queen. The source colony was split into three colonies, allocating roughly equal quantities of adult bees, brood, and pollen and nectar stores. One colony retained the original queen (QR), one was left queenless (QL), and the third was given a strip that contained 10 Qeq (QMP+), a dose shown to mimic a live queen (20). The three colonies were transferred to a different apiary > 2 mi away so they would not return to the site of their natal hive. Prior to the colony split, bees (N ~1500) were collected 0-36 h after eclosion, marked on the dorsal thorax with a paint dot (Testors Paint), and ~500 were placed in each of the three colonies. Two days later, the marked bees were collected (N = 100). Bees were collected into liquid nitrogen, and heads were stored as above.
2004-10-15 | E-MEXP-80 | biostudies-arrayexpress
Project description:Interactions between hosts and parasites have been hypothesized to cause winnerless coevolution, called Red Queen dynamics. The canonical Red Queen dynamics assume that all interacting genotypes of hosts and parasites undergo cyclic changes in abundance through negative frequency-dependent selection, which means that any genotype could become frequent at some stage. However, this prediction cannot explain why many rare genotypes stay rare in natural host-parasite systems. To investigate this, we build a mathematical model involving multihost and multiparasite genotypes. In a deterministic and controlled environment, Red Queen dynamics occur between two genotypes undergoing cyclic dominance changes, whereas the rest of the genotypes remain subordinate for long periods of time in phase-locked synchronized dynamics with low amplitude. However, introduction of stochastic noise in the model might allow the subordinate cyclic host and parasite types to replace dominant cyclic types as new players in the Red Queen dynamics. The factors that influence such evolutionary switching are interhost competition, specificity of parasitism, and degree of stochastic noise. Our model can explain, for the first time, the persistence of rare, hardly cycling genotypes in populations (for example, marine microbial communities) undergoing host-parasite coevolution.
| S-EPMC4783124 | biostudies-literature