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

The study investigates how plant viral infection influences the thermal biology of host plants and aphid vectors, and how these effects shape ecological interactions and interspecific competition between two aphid species, Rhopalosiphum padi and R. maidis. Vector-borne pathogens often manipulate host and vector phenotypes, affecting behaviors, host quality, and transmission dynamics. The authors hypothesize that barley yellow dwarf virus (BYDV) can modify plant surface temperatures and aphid thermal tolerance, thereby altering aphid spatial distribution on plants, competitive outcomes, and performance (lifespan and fecundity). The work focuses on two BYDV strains with distinct vector associations (BYDV-PAV with R. padi and BYDV-RMV with R. maidis) to determine strain- and species-specific thermal and ecological effects.

Prior research shows that pathogens can manipulate host and vector phenotypes to enhance transmission, including altering vector feeding behavior and host-derived sensory cues such as odors. Infection can also change host physiological traits (e.g., acclimation and defense chemistry), affecting host quality for vectors and influencing feeding dynamics and transmission. There is growing recognition that pathogen-induced phenotypic changes can extend to community-level interactions, yet implications for interspecific competition and microhabitat use remain less explored. Thermal heterogeneity on plant surfaces and species-specific thermal tolerances can structure aphid microhabitat partitioning and competition. BYDV interactions with aphids and symbiont-derived heat-shock proteins have been implicated in virus binding and potential stress responses, motivating examination of heat tolerance mechanisms.

- Study system: Two aphid species (Rhopalosiphum padi and R. maidis) and two BYDV strains: BYDV-PAV (vector: R. padi) and BYDV-RMV (vector: R. maidis). Host plants primarily wheat (field and lab), with aphid colonies maintained under controlled conditions. - Field thermal profiling: Infrared (IR) thermal imaging of wheat plants to quantify surface temperature differences among plant regions (e.g., stems vs. flag leaves). In field images, upper regions were warmer than stems (Student’s t = 47.41, df = 17, P ≤ 0.0001; n = 20 plants). - Laboratory plant thermal imaging: Compared virus-infected and control plants (dry, wet, untouched controls) using IR imaging; lab experiments used n = 6 plants per treatment; analyzed with Kruskal–Wallis tests. - Field distribution experiment: Full-factorial manipulation of aphid species presence (alone vs. co-occurring) and plant infection status (BYDV-PAV, BYDV-RMV, virus-free). Recorded aphid positions and associated temperatures; strong correlation between plant height and temperature at aphid locations (r² = 0.893). Nonparametric ANOVA (Kruskal–Wallis) assessed effects on occupied temperature and height (n = 10 plants per treatment). - Thermal tolerance assays (CTmax): Assessed upper temperature limit for locomotion using a metal capsule on an automated ceramic hotplate. Compared virus-free vs. viruliferous aphids. Sample size: n = 30 aphids per treatment. Student’s t-tests used. - Mortality under heat (LT50): Determined temperatures causing 50% mortality for virus-free vs. viruliferous aphids (Supplementary Fig. 2). - Locomotor performance: Measured movement speed at 14, 18, 22, 26, 30, and 36 °C in a walk-in climate chamber; compared species and infection statuses (Supplementary Fig. 3). - Thermal preference on plants: Created thermal gradients on wheat using electrical resistances; quantified preferred microhabitat temperatures for each species and infection status (Supplementary Fig. 4). - Gene expression: Extracted mRNA from virus-free and BYDV-PAV-infected R. padi at room temperature (23 °C) and at CTmax. Constructed transcriptome libraries (Illumina) and validated candidate heat-shock genes via qRT-PCR (n = 8 per treatment). Expression levels compared to virus-free, no-heat controls using t-tests. - Life-history experiments: Full-factorial design manipulating temperature (15–28 °C), viral infection (BYDV-PAV, BYDV-RMV, or virus-free), and interspecific competition (alone vs. co-occurring) in climate-controlled chambers. Measured adult lifespan and fecundity (n = 15 per treatment per temperature). Statistical analyses used ANOVA/GLM frameworks (including Kruskal–Wallis and generalized linear models with appropriate error structures).

- Virus-induced plant warming: BYDV infection increased plant surface temperatures by about 2 °C; upper plant regions (flag leaves) were significantly warmer than stems (field t = 47.41, df = 17, P ≤ 0.0001; n = 20 plants). - Aphid microhabitat and competition: Plant height strongly correlated with temperature at aphid locations (r² = 0.893). When co-occurring with R. maidis, R. padi shifted upward on the plant to warmer regions, occupying sites ~4 °C hotter on average; R. maidis’ distribution was largely unaffected by R. padi. - Thermal tolerance (CTmax): BYDV-PAV infection increased R. padi CTmax by 8 °C relative to virus-free individuals (n = 30 per treatment; significant by t-test). BYDV-RMV did not significantly change R. maidis CTmax. - Mortality under heat: BYDV-PAV increased LT50 (temperature causing 50% mortality) for R. padi (Supplementary Fig. 2). - Locomotion: At low temperatures (14–18 °C), R. maidis moved faster than R. padi regardless of infection; at higher temperatures (26–35 °C), viruliferous R. padi achieved the highest speeds. Viruliferous R. maidis showed no comparable high-temperature increase. - Thermal preferences: R. padi selected microhabitats ~3 °C warmer than R. maidis on thermal-gradient plants; viral infection did not alter these preferences (Supplementary Fig. 4). - Gene expression: BYDV-PAV-infected R. padi showed increased expression of heat-shock protein genes (e.g., Hsp70 A and Hsp70 B significantly upregulated; t = 9.81 and 6.45, df = 34, P < 0.0001), consistent with enhanced heat tolerance (Fig. 4). - Life-history effects: Temperature, virus, and co-occurrence significantly affected R. padi lifespan and fecundity (e.g., Table: Temp χ² = 510.23, P < 0.0001; Virus χ² = 65.69, P < 0.0001). In the absence of infection/competition, increasing temperature (15→28 °C) tripled R. padi lifespan but halved R. maidis lifespan. Competition reduced lifespan for both species: presence of R. padi reduced R. maidis lifespan by ~10 days at 15–21 °C; presence of R. maidis reduced R. padi lifespan by 2–5 days across temperatures. Viral infection increased lifespan and fecundity in both species, with strong magnitude at 23 °C: fecundity increased by ~320% for R. padi and ~230% for R. maidis on infected plants; R. padi lifespan increased by up to ~20% (BYDV-PAV). Virus benefits mitigated negative competition effects. - Overall: BYDV-PAV both warms host plants and enhances R. padi thermal tolerance, enabling upward, warmer microhabitat use when competing with R. maidis, effectively expanding R. padi’s fundamental niche.

The findings demonstrate a dual thermal effect of BYDV-PAV: it elevates host plant surface temperatures and increases the heat tolerance of its vector, R. padi. These effects alter interspecific interactions and microhabitat use, allowing the smaller R. padi to occupy warmer, higher plant strata when displaced from cooler zones by the larger R. maidis. Enhanced heat tolerance correlates with upregulation of heat-shock protein genes, providing a plausible physiological mechanism. In contrast, BYDV-RMV did not measurably increase R. maidis thermal tolerance, underscoring strain- and vector-specific outcomes. Viral infection improved aphid lifespan and fecundity—especially for R. padi under warmer conditions—reducing the negative impacts of competition and potentially enhancing virus transmission through increased vector performance. These results highlight the importance of pathogen-induced thermal phenotype changes for structuring communities and shaping vector-host-nonvector interactions, with broader implications for disease ecology in thermally heterogeneous environments.

BYDV-PAV increases host plant temperatures and markedly enhances the thermal tolerance of its vector, R. padi, via upregulation of heat-shock protein genes. This enables R. padi to exploit warmer microhabitats on infected plants under interspecific competition, expanding its fundamental niche. Viral infection simultaneously elevates aphid lifespan and fecundity, mitigating competition effects and likely promoting virus transmission. The study reveals that pathogen effects on thermal biology can restructure ecological interactions among hosts, vectors, and competitors. Future research should elucidate the plant physiological mechanisms underlying virus-induced warming (e.g., stomatal regulation), dissect the molecular pathways linking virus presence to aphid Hsp expression (including roles of endosymbiont chaperones), test generality across host plants and environments, and evaluate implications under climate warming.

- Mechanisms underlying virus-induced increases in plant surface temperature remain unresolved (e.g., stomatal or signaling changes are hypothesized but untested). - Gene expression analyses focused on R. padi; comparable molecular data for R. maidis were not presented, limiting cross-species inference. - Some experiments used controlled laboratory settings and engineered thermal gradients, which may not fully capture natural thermal variability. - Results are specific to two BYDV strains and two aphid species on cereal hosts; generalization to other host–vector systems requires further testing. - While performance effects were strong, potential density-dependent resource limitations and long-term population dynamics were not directly measured.