Enhanced heat tolerance of viral-infected aphids leads to niche expansion and reduced interspecific competition

Abstract

Vector-borne pathogens are known to alter the phenotypes of their primary hosts and vectors, with implications for disease transmission as well as ecology. Here we show that a plant virus, barley yellow dwarf virus, increases the surface temperature of infected host plants (by an average of 2°C), while also significantly enhancing the thermal tolerance of its aphid vector Rhopalosiphum padi (by 8°C). This enhanced thermal tolerance, which was associated with differential upregulation of three heat-shock protein genes, allowed aphids to occupy higher and warmer regions of infected host plants when displaced from cooler regions by competition with a larger aphid species, R. maidis. Infection thereby led to an expansion of the fundamental niche of the vector. These findings show that virus effects on the thermal biology of hosts and vectors can influence their interactions with one another and with other, non-vector organisms.

Effect of Banana Bunchy Top Virus on the Heat Shock Protein Genes of Pentalonia nigronervosa during Temperature Susceptibility and Its Effect on Virus Transmission

“…Reports also indicated alterations in several Hsps in B.tabaci under thermal stress conditions (40 • C or 44 • C) [48]. However, several contradictory reports have been addressed where thermal tolerance in Rhopalosiphum padi appears to increase with the acquisition of barley yellow dwarf virus (BYDV), leading to an expansion of the thermal niche of the vector [49]. It has also been reported in Southern rice black-streaked dwarf virus, which increases heat tolerance in its vector, Sogatella furcifera [50].…”

“…However, when the experiment was conducted for only 2 h or 24 h, the virus showed 100% transmission rate. Such observations may be due to the reduced activity of the aphid vector at low temperatures [49]. In addition, the increased mortality of adult aphids at lower temperatures can also be a potential reason for such inefficiency in transmission.…”

Microbes increase thermal sensitivity in the mosquito Aedes aegypti, with the potential to change disease distributions

“…aegypti infected with the wMel strain of Wolbachia exhibit reduced maternal transmission rates in response to heat spikes that can lead to the production of uninfected offspring [36]. More recently, several studies in Drosophila species have demonstrated that Wolbachia infection can change the host insect's thermal preference [37], of which the directionality varies by bacterial strain [38] More broadly, infection in invertebrates has been shown to substantially increase host or vector susceptibility to thermal stress [39][40][41][42]. A recent study conducted by Hector et al, 2019 showed that Daphnia magna (water flea) infected with the bacterial pathogen Pasteuria ramosa exhibit a reduction in thermal limits up to 2˚C.…”

Thermal limits in the face of infectious disease: How important are pathogens?

“…However, there is no doubt that there is the potential for infection to impact the thermal performance of other organisms which play a key role in ecosystems and community structures, including plants. Both infection and thermal stress are likely to shape the response of plants to environmental change, with the potential for antagonistic or correlated responses to the two stressors (Desaint et al, 2021; González et al, 2020; Márquez et al, 2007; Pandey et al, 2015; Porras et al, 2020). For example, heat stress can lead to either greater susceptibility or resistance to disease in multiple plant systems depending on the species in question (Pandey et al, 2015), suggesting that infection may in turn have a variable impact on the performance of host plants exposed to extreme temperatures.…”