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Molecular evolution of juvenile hormone esterase-like proteins in a socially exchanged fluid

ABSTRACT: Socially exchanged fluids, such as seminal fluid and milk, are a direct means through which an organism can influence conspecifics. When orally feeding larval offspring via trophallaxis, workers of the carpenter ant Camponotus floridanus were recently shown to transfer Juvenile Hormone III (JH), a key developmental regulator, as well as paralogs of JH esterase (JHE), an enzyme that catalyzes degradation of JH. Here we combine proteomic, phylogenetic and selection analyses to investigate the evolution of this esterase subfamily. We show that members of the Camponotus JHE-like protein family have undergone multiple duplications, experienced positive selection, and changed tissue localization to become abundantly and selectively present in trophallactic fluid. The Camponotus trophallactic esterases have maintained their catalytic triads but contain a number of positively-selected amino acid changes distributed throughout the protein, which possibly reflect an adaptation to the highly acidic trophallactic fluid of formicine ants. To determine whether these esterases might regulate larval development, we fed workers with a JHE-specific pharmacological inhibitor to introduce it into the trophallactic network. This inhibitor increased the likelihood of pupation of the larvae reared by these workers, similar and complementary to supplementation with JH. Together, these findings suggest that JHE-like proteins have evolved new roles in the Camponotus genus in inter-individual regulation of larval development.

INSTRUMENT(S): LTQ Orbitrap, LTQ Orbitrap Velos

ORGANISM(S): Camponotus Floridanus

TISSUE(S): Whole Body

SUBMITTER: Patrice Waridel

LAB HEAD: Laurent Keller

PROVIDER: PXD009982 | Pride | 2018-12-14

REPOSITORIES: Pride

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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

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Molecular evolution of juvenile hormone esterase-like proteins in a socially exchanged fluid

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