Behavioural manipulation of insect hosts by Baculoviridae as a process of niche construction

Mark M Tanaka,Steven Hamblin

doi:10.1186/1471-2148-13-170

Abstract

BackgroundNiche construction has received increasing attention in recent years as a vital force in evolution and examples of niche construction have been identified in a wide variety of taxa, but viruses are conspicuously absent. In this study we explore how niche construction can lead to viruses engineering their hosts (including behavioural manipulation) with feedback on selective pressures for viral transmission and virulence. To illustrate this concept we focus on Baculoviridae, a family of invertebrate viruses that have evolved to modify the feeding behaviour of their lepidopteran hosts and liquefy their cadavers as part of the course of infection.ResultsWe present a mathematical model showing how niche construction leads to feedback from the behavioural manipulation to the liquefaction of the host, linking the evolution of both of these traits, and show how this association arises from the action of niche construction. Model results show that niche construction is plausible in this system and delineates the conditions under which niche construction will occur. Niche construction in this system is also shown to be sensitive to parameter values that reflect ecological forces.ConclusionsOur model demonstrates that niche construction can be a potent force in viral evolution and can lead to the acquisition and maintenance of the behavioural manipulation and liquefaction traits in Baculoviridae via the niche constructing effects on the host. These results show the potential for niche construction theory to provide new insights into viral evolution.

Highlights

Niche construction has received increasing attention in recent years as a vital force in evolution and examples of niche construction have been identified in a wide variety of taxa, but viruses are conspicuously absent
Mathematical model of viral niche construction Epizootic model To study the effects of baculovirus behavioural manipulation and liquefaction on viral fitness, we begin with a compartmental epizootic model similar to a SusceptibleExposed-Infectious-Recovered (SEIR) model [21]
We focus on the dynamics of acute infection by baculovirus of a local population of larval hosts and consider long-term niche construction arising from these dynamics

Summary

Introduction

Niche construction has received increasing attention in recent years as a vital force in evolution and examples of niche construction have been identified in a wide variety of taxa, but viruses are conspicuously absent. Niche construction, defined as the “process whereby organisms, through their metabolism, their activities, and their choices, modify their own and/or each other’s niches” [1], has received growing attention as a potentially potent force in evolution This act of modifying niches changes biotic and abiotic sources of selection in the organisms’s environment, introducing feedback into the evolutionary process as the effects of niche construction modify an organism’s genetic and ecological inheritance [2,3]. Viruses even have lasting effects on the environment beyond the host, as when marine viruses affect oceanic participation in carbon cycling [7] This process of modifying the host may change the host’s selective pressures; beyond the response of the immune system, the host may be under selection to counter the effects of the physiological or behavioural manipulations of the virus. With their short generation time and quick rates of evolution, viruses are attractive targets for empirical tests of niche construction theory

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