Differential impacts of juvenile hormone, soldier head extract and alternate caste phenotypes on host and symbiont transcriptome composition in the gut of the termite Reticulitermes flavipes.

Ruchira Sen,Rhitoban Raychoudhury,Drion G Boucias,Verena-Ulrike Lietze,Michael E Scharf,Yunpeng Cai,Yijun Sun

doi:10.1186/1471-2164-14-491

Abstract

BackgroundTermites are highly eusocial insects and show a division of labor whereby morphologically distinct individuals specialize in distinct tasks. In the lower termite Reticulitermes flavipes (Rhinotermitidae), non-reproducing individuals form the worker and soldier castes, which specialize in helping (e.g., brood care, cleaning, foraging) and defense behaviors, respectively. Workers are totipotent juveniles that can either undergo status quo molts or develop into soldiers or neotenic reproductives. This caste differentiation can be regulated by juvenile hormone (JH) and primer pheromones contained in soldier head extracts (SHE). Here we offered worker termites a cellulose diet treated with JH or SHE for 24-hr, or held them with live soldiers (LS) or live neotenic reproductives (LR). We then determined gene expression profiles of the host termite gut and protozoan symbionts concurrently using custom cDNA oligo-microarrays containing 10,990 individual ESTs.ResultsJH was the most influential treatment (501 total ESTs affected), followed by LS (24 ESTs), LR (12 ESTs) and SHE treatments (6 ESTs). The majority of JH up- and downregulated ESTs were of host and symbiont origin, respectively; in contrast, SHE, LR and LS treatments had more uniform impacts on host and symbiont gene expression. Repeat “follow-up” bioassays investigating combined JH + SHE impacts in relation to individual JH and SHE treatments on a subset of array-positive genes revealed (i) JH and SHE treatments had opposite impacts on gene expression and (ii) JH + SHE impacts on gene expression were generally intermediate between JH and SHE.ConclusionsOur results show that JH impacts hundreds of termite and symbiont genes within 24-hr, strongly suggesting a role for the termite gut in JH-dependent caste determination. Additionally, differential impacts of SHE and LS treatments were observed that are in strong agreement with previous studies that specifically investigated soldier caste regulation. However, it is likely that gene expression outside the gut may be of equal or greater importance than gut gene expression.

Highlights

Termites are highly eusocial insects and show a division of labor whereby morphologically distinct individuals specialize in distinct tasks
Experimental application of juvenile hormone (JH) to workers of different social insects has been shown to induce two major types of changes; such as (i) stimulating young workers to carry out functions that are usually performed by older individuals [3] or (ii) inducing workers to go through physical changes and differentiate from one phenotype to another [4]
We focused on worker termites because in lower termites like R. flavipes (i) workers compose >90% of colonies, (ii) their guts house both eukaryotic and prokaryotic symbionts, (iii) they are responsible for the majority of lignocellulose digestion, and (iv) workers are totipotent juveniles that retain the capacity to differentiate into both soldier and reproductive caste phenotypes [1,20,29,30]

Summary

Introduction

Termites are highly eusocial insects and show a division of labor whereby morphologically distinct individuals specialize in distinct tasks. Workers are totipotent juveniles that can either undergo status quo molts or develop into soldiers or neotenic reproductives This caste differentiation can be regulated by juvenile hormone (JH) and primer pheromones contained in soldier head extracts (SHE). Are carried out by individuals, which are often differentiated into worker sub-castes that each performs specific duties Such differentiation is either morphological, where physical features determine the tasks (polyphenism), or age-based, where workers carry out different functions at different ages (polyethism) [1]. In both types of caste differentiation, juvenile hormone (JH) is known to play a significant role in most social insects [2]. Aside from two caste-regulatory genes and two soldier-derived primer pheromones linked to presoldier caste regulation [5,6,7], relatively little is known about the molecular mechanisms of caste differentiation in termites and the factors that initiate this process

Methods

Results

Discussion

Conclusion