Pleiotropic effects of juvenile hormone in ant queens and the escape from the reproduction-immunocompetence trade-off.
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ABSTRACT:
SUBMITTER: Pamminger T
PROVIDER: S-EPMC4721097 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The question on how individuals allocate resources into maintenance and reproduction is one of the central questions in life history theory. Yet, resource allocation into maintenance on the organismic level can only be measured indirectly. This is different in a social insect colony, a "superorganism" where workers represent the soma and the queen the germ line of the colony. Here, we investigate whether trade-offs exist between maintenance and reproduction on two levels of biological organization, queens and colonies, by following single-queen colonies of the ant Cardiocondyla obscurior throughout the entire lifespan of the queen. Our results show that maintenance and reproduction are positively correlated on the colony level, and we confirm results of an earlier study that found no trade-off on the individual (queen) level. We attribute this unexpected outcome to the existence of a positive feedback loop where investment into maintenance (workers) increases the rate of resource acquisition under laboratory conditions. Even though food was provided ad libitum, variation in productivity among the colonies suggests that resources can only be utilized and invested into additional maintenance and reproduction by the colony if enough workers are available. The resulting relationship between per-capita and colony productivity in our study fits well with other studies conducted in the field, where decreasing per-capita productivity and the leveling off of colony productivity have been linked to density dependent effects due to competition among colonies. This suggests that the absence of trade-offs in our laboratory study might also be prevalent under natural conditions, leading to a positive association of maintenance, (= growth) and reproduction. In this respect, insect colonies resemble indeterminate growing organisms.
| S-EPMC4575186 | biostudies-literature
Project description:Life-history theory predicts a trade-off between reproductive investment and self-maintenance. The negative association between fertility and longevity found throughout multicellular organisms supports this prediction. As an important exception, the reproductives of many eusocial insects (ants, bees, and termites) are simultaneously very long-lived and highly fertile. Here, we examine the proximate basis for this exceptional relationship by comparing whole-body transcriptomes of differently aged queens of the ant Cardiocondyla obscurior. We show that the sets of genes differentially expressed with age significantly overlap with age-related expression changes previously found in female Drosophila melanogaster. We identified several developmental processes, such as the generation of neurons, as common signatures of aging. More generally, however, gene expression in ant queens and flies changes with age mainly in opposite directions. In contrast to flies, reproduction-associated genes were upregulated and genes associated with metabolic processes and muscle contraction were downregulated in old relative to young ant queens. Furthermore, we searched for putative C. obscurior longevity candidates associated with the previously reported lifespan-prolonging effect of mating by comparing the transcriptomes of queens that differed in mating and reproductive status. We found 21 genes, including the putative aging candidate NLaz (an insect homolog of APOD), which were consistently more highly expressed in short-lived, unmated queens than in long-lived, mated queens. Our study provides clear evidence that the alternative regulation of conserved molecular pathways that mediate the interplay among mating, egg laying, and aging underlies the lack of the fecundity/longevity trade-off in ant queens.
| S-EPMC5009957 | biostudies-literature
Project description:In honeybees, differential feeding of female larvae promotes the occurrence of two different phenotypes, a queen and a worker, from identical genotypes. Nutritional factors affect both endocrine responses and gene expression and, thus, change the larval developmental pattern. It is widely accepted that two types of alterations occur during this process: incremental alterations, which affect general growth, and character state alterations that result in the presence or absence of specific structures. Previous studies revealed a link between incremental alterations and differential expression of physiometabolic genes. Here, we report evidence for molecular changes that affect character states, controlling the expression of worker-like characteristics. By using cDNA microarray analyses of more than 6,000 Apis mellifera ESTs we found 240 differentially expressed genes (DEG) between developing queens and workers. Comparative analyses showed that many genes recorded as up-regulated in prospective workers appear to be unique to A. mellifera suggesting that the workers developmental pathway involves the participation of novel genes. We also show that workers up-regulate more developmental genes than queens, whereas queens up-regulate a greater predominance of physiometabolic genes. The latter include genes coding for metabolic enzymes and genes whose products are known to regulate the rate of mass-transforming processes and the general growth of the organism (e.g., tor). Many DEG are likely to be involved in processes favoring the development of caste-specific structures, like brain, legs and ovaries, as well as genes that code for cytoskeleton constituents. Treatment of developing worker larvae with juvenile hormone (JH) revealed 52 JH responsive genes, specifically during the critical period of castes development. Using Gibbs sampling and Expectation Maximization algorithms, we discovered eight overrepresented cis-elements from 4 gene groups. Graph theory and complex networks concepts were adopted to attain powerful graphical representations of the interrelation between cis-elements and genes and objectively quantify the degree of relationship between these entities. We suggest that clusters of functionally related DEGs are co-regulated during caste development in honeybees. This network of interactions is activated by nutrition-driven stimuli in early larval stages. Our data are consistent with the hypothesis that JH is a key component of the developmental determination of queen-like characters. We propose a conceptual model of caste differentiation in A. mellifera based on gene-regulatory networks. Keywords: caste differentiation during larval development; JH effect
2007-05-31 | GSE6452 | GEO
Project description:In many cooperatively breeding animals, subordinate group members have lower reproductive capacity than dominant group members. Theory suggests subordinates may downregulate their reproductive capacity because dominants punish subordinates who maintain high fertility. However, there is little direct experimental evidence that dominants cause physiological suppression in subordinates. Here, we experimentally test how social interactions influence subordinate reproductive hormones in Polistes dominula paper wasps. Polistes dominula queens commonly found nests in cooperative groups where the dominant queen is more fertile than the subordinate queen. In this study, we randomly assigned wasps to cooperative groups, assessed dominance behaviour during group formation, then measured levels of juvenile hormone (JH), a hormone that mediates Polistes fertility. Within three hours, lowest ranking subordinates had less JH than dominants or solitary controls, indicating that group formation caused rapid JH reduction in low-ranking subordinates. In a second experiment, we measured the behavioural consequences of experimentally increasing subordinate JH. Subordinates with high JH-titres received significantly more aggression than control subordinates or subordinates from groups where the dominant's JH was increased. These results suggest that dominants aggressively punished subordinates who attempted to maintain high fertility. Low-ranked subordinates may rapidly downregulate reproductive capacity to reduce costly social interactions with dominants. Rapid modulation of subordinate reproductive physiology may be an important adaptation to facilitate the formation of stable, cooperative groups.
| S-EPMC5829203 | biostudies-literature
Project description:Cooperative breeding animals frequently inhabit harsh environments. It is widely accepted that harsh environments hinder independent reproduction, and this constraint maintains individuals in family groups. Yet the assumption that harsh ecological conditions reduce the success of members of cooperative breeding groups when breeding independently has not been experimentally tested. We addressed this shortcoming using the socially polymorphic Alpine silver ant, Formica selysi. This species has single-queen (independent breeders) and multiple-queen (cooperative breeders) colonies coexisting within populations. We placed newly mated queens emerging from each type of colony to breed alone in either a harsh or mild winter condition and recorded their brood production and survival. Queens emerging from single-queen colonies were unaffected by the winter condition and were more successful at founding a nest independently than queens from multiple-queen colonies. By contrast, queens from multiple-queen colonies had higher mortality after a harsh than after a mild winter. These results support the long-held assumption that harsh environments constrain independent reproduction of members of cooperative breeding groups.
| S-EPMC7013492 | biostudies-literature
Project description:Will be added/updated once the manuscript is finalized.
2013-10-26 | GSE24953 | GEO
Project description:Reproductive sharing in animal groups with multiple breeders, insects and vertebrates alike, contains elements of both conflict and cooperation, and depends on both relatedness between co-breeders, as well as their internal and external conditions. We studied how queens of the ant Formica fusca adjust their reproductive efforts in response to experimental manipulations of the kin competition regime in their nest. Queens respond to the presence of competitors by increasing their egg laying efforts, but only if the competitors are highly fecund and distantly related. Such a mechanism is likely to decrease harmful competition among close relatives. We demonstrate that queens of Formica fusca fine-tune their cooperative breeding behaviors in response to kinship and fecundity of others in a remarkably precise and flexible manner.
| S-EPMC10183207 | biostudies-literature
Project description:Social insects provide ideal systems for investigating how kinship and ecological factors affect cooperation and conflict. In many ant species, unrelated queens cooperate to initiate new colonies. However, fights between queens break out after the eclosion of the first workers, leading to the death of all but one queen. Queens within associations potentially face a trade-off. On one hand, a queen should restrain her investment in brood production and care if this helps her to maintain fighting ability. On the other hand, a queen may benefit by increasing her contribution to brood production if having more daughter workers than her cofoundresses enhances her chances of taking over the colony. Increased investment is also beneficial because a large brood enhances colony survival. Using microsatellites, we determined the maternity of workers (adults and larvae) at the time of queen execution in the fire ant, Solenopsis invicta. Differential mass loss by initially equal nestmates affected survival, with the queen losing less body mass being more likely to survive. Surprisingly, the queen which lost less body mass, that is the one which provided the lowest energy investment, was the one which achieved higher maternity. A control experiment indicated that interactions among queens are responsible for this differential partitioning of reproductive and investment tasks between nestmates. The finding that the queen most likely to win the fights is the one with above-average maternity may explain why workers apparently do not attempt to influence the outcome of fights.
| S-EPMC1688589 | biostudies-other
Project description:The behavioral traits that shape the structure of animal societies vary considerably among species but appear to be less flexible within species or at least within populations. Populations of the ant Leptothorax acervorum differ in how queens interact with other queens. Nestmate queens from extended, homogeneous habitats tolerate each other and contribute quite equally to the offspring of the colony (polygyny: low reproductive skew). In contrast, nestmate queens from patchy habitats establish social hierarchies by biting and antennal boxing, and eventually only the top-ranking queen of the colony lays eggs (functional monogyny: high reproductive skew). Here we investigate whether queen-queen behavior is fixed within populations or whether aggression and high skew can be elicited by manipulation of socio-environmental factors in colonies from low skew populations. An increase of queen/worker ratio and to a lesser extent food limitation elicited queen-queen antagonism in polygynous colonies from Nürnberger Reichswald similar to that underlying social and reproductive hierarchies in high-skew populations from Spain, Japan, and Alaska. In manipulated colonies, queens differed more in ovarian status than in control colonies. This indicates that queens are in principle capable of adapting the magnitude of reproductive skew to environmental changes in behavioral rather than evolutionary time.
| S-EPMC3990625 | biostudies-literature
Project description:Pyriproxyfen is an insecticidal juvenile hormone analog that perturbs insect and tick development. Pyriproxyfen also alters parthenogenic reproduction in non-target cladoceran species as it induces male production that can lead to a decrease in fecundity, a reduction in population density, and subsequent ecological effects. In this study, we investigate the impacts of pyriproxyfen on Daphnia magna reproduction using a series of male production screening assays. These assays demonstrate that pyriproxyfen increases male production in a concentration-dependent fashion with an EC50 of 156pM (50.24ngL(-1)); a concentration considered environmentally relevant. Furthermore, pyriproxyfen decreases overall fecundity at all ages tested (7, 14, 21-d old female parthenogenic daphnids). Juvenile (3-d old) and reproductively mature (10-d old) female daphnids were also exposed to 155pM pyriproxyfen for 2-12d and reproduction measured for 16d to compare the effects of short-term and prolonged exposures, and determine the potential for recovery. Results indicate that longer pyriproxyfen exposures (8-12d) extend male production and decrease reproduction; however, daphnids exposed for only 2-4d recover and produce a relatively normal abundance of neonates. In addition, juvenile daphnids are also very sensitive to pyriproxyfen, but the primary effect on juvenile daphnids is reduced reproduction and protracted development not male production. Taken together, continued use of pyriproxyfen around water bodies needs due caution because of its potential adverse effects with significant developmental delays and male production compounded by prolonged exposure.
| S-EPMC3716864 | biostudies-literature