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

Abstract

Socially exchanged fluids are a direct means by which an organism can influence conspecifics. It was recently shown that when workers of the carpenter ant Camponotus floridanus feed larval offspring via trophallaxis, they transfer Juvenile Hormone III (JH), a key developmental regulator, as well as paralogs of JH esterase (JHE), an enzyme that catalyzes the hydrolysis of JH. Here we combine proteomic, phylogenetic and selection analyses to investigate the evolution of this esterase subfamily. We show that Camponotus JHE-like proteins 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 and 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 to the influence of food supplementation with JH. Together, these findings suggest that JHE-like proteins have evolved a new role in the inter-individual regulation of larval development in the Camponotus genus.

Genetic Underpinnings of Host Manipulation byOphiocordycepsas Revealed by Comparative Transcriptomics

“…Insulin/insulin-like growth factor (IGF) signaling (IIS) pathways have been implicated in behavior, division of labor, and establishment of reproductive caste and associated behaviors in ants and bees ( Ament et al 2008 ; Chandra et al 2018 ). Juvenile hormone and vitellogenin (VG) appear to play an important role in IIS pathways and behavior, although typically the strongest effects are observed during development and early life ( Bloch et al 2000 ; Brent et al 2006 ; Lengyel et al 2006 ; Nelson et al 2007 ; Ament et al 2008 , 2010 ; Velarde et al 2009 ; Penick et al 2011 ; Dolezal et al 2012 ; Libbrecht et al 2013 ; Corona et al 2013 , 2016; Das 2016 ; Chandra et al 2018 ; LeBoeuf et al 2018 ; Opachaloemphan et al 2018 ). Nutritional status, energy demands, and behaviors such as foraging appear to be interlinked in these eusocial insects.…”

Transcriptomic basis and evolution of the ant nurse-larval social interactome

“…In many taxa including certain birds, mammals, and insects, care for offspring and the regulation of offspring development has shifted at least in part from parents to adult siblings, who perform alloparental care [11]. In eusocial insect societies, sterile nurse workers regulate the development of their larval siblings by modulating the quantity and quality of nourishment larvae receive [12–14], as well as through the direct transfer of growth-regulating hormones and proteins [15,16]. At the same time, larvae influence nurse provisioning behavior via pheromones [17–20] and begging behavior [21,22].…”

“…depends on the combination of larval and nurse genotypes [28–34]. However, the identity of specific genes and molecular pathways that are functionally involved in the expression of social interactions (e.g., genes underlying nurse and larval traits affecting nurse-larva interactions) and the patterns of molecular evolution for these genes have remained less well studied [15,16,35,36].…”

Dual‐fluorescence imaging and automated trophallaxis detection for studying multi‐nutrient regulation in superorganisms

“…In a broader view, with empirical access to the flows of nutrients in a colony, one may study the properties and functions of ant food-sharing networks while varying different ecologically-relevant parameters, such as food source availability or quality, predation risk and competition. Furthermore, tracking different materials in the trophallactic fluid is expected to be useful in other contemporary research subjects, including: the trade-offs between food and pathogen transmission through contact networks (Sendova-Franks et al, 2010;Stroeymeyt et al, 2018;Csata and Dussutour, 2019), the different nutritional needs within colonies and their close symbionts (Crumière et al, 2020), the control of microbial communities ingested with food (Sclocco and Teseo, 2020), and regulatory effects of trophallactic fluid on differential larval development (LeBoeuf, Waridel, et al, 2016;LeBoeuf, Cohanim, et al, 2018). Importantly, this method can potentially be applicable to other trophallaxis-This article is protected by copyright.…”