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Rapid juvenile hormone downregulation in subordinate wasp queens facilitates stable cooperation.

ABSTRACT: 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.

SUBMITTER: Tibbetts EA

PROVIDER: S-EPMC5829203 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Rapid juvenile hormone downregulation in subordinate wasp queens facilitates stable cooperation.

Tibbetts Elizabeth A EA Fearon Michelle L ML Wong Ellery E Huang Zachary Y ZY Tinghitella Robin M RM

Proceedings. Biological sciences 20180201 1872

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 <i>Polistes d ...[more]

PMID: 29436498

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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

Project description:AbstractKey social traits, like queen number in eusocial insect colonies, have long been considered plastic, but the recent finding that colony social organization is under strict genetic control in multiple ant lineages challenges this view. This begs the question of which hardwired behavioral mechanism(s) generate alternative forms of social organization during colony development. We addressed this question in the Alpine silver ant, Formica selysi, a species with two social forms determined by a supergene. Queens that carry exclusively the M haplotype are produced by and live in monogyne (= single-queen) colonies, whereas queens that carry at least one copy of the P haplotype are produced by and live in polygyne (= multiple-queen) colonies. With extensive field samplings and laboratory experiments, we show that both types of queens successfully establish colonies independently, without being accompanied by workers, but that they do so in contrasting ways. Monogyne queens were generally intolerant of other queens and founded colonies solitarily, whereas polygyne queens were mutually attracted to each other and mainly founded colonies cooperatively. These associations persisted for months after worker emergence, suggesting that cooperative colony-founding leads to permanent multiple queening. Overall, our study shows that queens of each social form found colonies independently in the field but that P-carrying queens are more likely to cooperate, thereby contributing to perpetuate alternative forms of social organization.Significance statementUnderstanding the genetic and behavioral underpinnings of social organization is a major goal in evolutionary biology. Recent studies have shown that colony social organization is controlled by supergenes in multiple ant lineages. But the behavioral processes linking the genotype of a queen to the type of colony she will form remain largely unknown. Here, we show that in Alpine silver ants, alternative supergene genotypes are associated with different levels of social attraction and tolerance in young queens. These hardwired differences in social traits make queens carrying the P supergene haplotype more prone to cooperate and form durable associations during independent colony-founding. These findings help explain how genetic variants induce alternative forms of social organization during the ontogeny of a colony. They also illustrate how simple phenotypic differences at the individual level can result in large differences at higher levels of organization.Supplementary informationThe online version contains supplementary material available at 10.1007/s00265-021-03105-1.

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Rapid juvenile hormone downregulation in subordinate wasp queens facilitates stable cooperation.

Publications

Rapid juvenile hormone downregulation in subordinate wasp queens facilitates stable cooperation.

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