Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity.

Marah Stoldt,Linda Klein,Barbara Feldmeyer,Susanne Foitzik,Evelien Jongepier,Falk Butter,Sara Beros

doi:10.3390/genes12010095

Abstract

Most species are either parasites or exploited by parasites, making parasite–host interactions a driver of evolution. Parasites with complex life cycles often evolve strategies to facilitate transmission to the definitive host by manipulating their intermediate host. Such manipulations could explain phenotypic changes in the ant Temnothorax nylanderi, the intermediate host of the cestode Anomotaenia brevis. In addition to behavioral and morphological alterations, infected workers exhibit prolonged lifespans, comparable to that of queens, which live up to two decades. We used transcriptomic data from cestodes and ants of different castes and infection status to investigate the molecular underpinnings of phenotypic alterations in infected workers and explored whether the extended lifespan of queens and infected workers has a common molecular basis. Infected workers and queens commonly upregulated only six genes, one of them with a known anti-aging function. Both groups overexpressed immune genes, although not the same ones. Our findings suggest that the lifespan extension of infected workers is not achieved via the expression of queen-specific genes. The analysis of the cestodes’ transcriptome revealed dominant expression of genes of the mitochondrial respiratory transport chain, which indicates an active metabolism and shedding light on the physiology of the parasite in its cysticercoid stage.

Highlights

Parasitism—life by exploiting resources from other living organisms—is one of the most fascinating life-history strategies in nature and used by the majority of species onEarth [1]
Some intriguing examples for host alterations are found in insects that serve as intermediate hosts, such as the neotropical ant Cephalotes atratus when infected by the nematode Myrmeconema neotropicum
To gain insights into the significance of infection status on the general gene expression pattern, we conducted a Principal Component Analysis (PCA) based on the overall read counts of these genes and tested the influence of infection status on each of the 16 principal components

Summary

Introduction

Parasitism—life by exploiting resources from other living organisms—is one of the most fascinating life-history strategies in nature and used by the majority of species onEarth [1]. Parasites with complex life cycles have developed a variety of strategies to facilitate the trophic transmission from the intermediate to the definitive host. They can achieve this by altering their host’s morphology, physiology, or behavior to their benefit [2]. Phenotypic alterations observed in infected insect hosts can include an extended host lifespan. A similar phenomenon is found in mice, where the parasitic nematode’s release of the molecule ES-62 extends the lifespan of this mammalian host by 70 days likely due to anti-inflammatory properties of the secretion [8]. Other parasites hijack the immune system like the parasitic wasp Cotesia congregate, which elicits an elevated octopamine level in the hemolymph of its host Manduca sexta similar to what is observed after an immune challenge [11,12]

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Conclusion