Assessing the role of family level variation and heat shock gene expression in the thermal stress response of the mosquito Aedes aegypti

Abstract

The geographical range of the mosquito vector for many human disease-causing viruses, Aedes aegypti, is expanding, in part owing to changing climate. The capacity of this species to adapt to thermal stress will affect its future distributions. It is unclear how much heritable genetic variation may affect the upper thermal limits of mosquito populations over the long term. Nor are the genetic pathways that confer thermal tolerance fully understood. In the short term, cells induce a plastic, protective response known as 'heat shock'. Using a physiological 'knockdown' assay, we investigated mosquito thermal tolerance to characterize the genetic architecture of the trait. While families representing the extreme ends of the distribution for knockdown time differed from one another, the trait exhibited low but non-zero broad-sense heritability. We then explored whether families representing thermal performance extremes differed in their heat shock response by measuring gene expression of heat shock protein-encoding genes Hsp26, Hsp83 and Hsp70. Contrary to prediction, the families with higher thermal tolerance demonstrated less Hsp expression. This pattern may indicate that other mechanisms of heat tolerance, rather than heat shock, may underpin the stress response, and the costly production of HSPs may instead signal poor adaptation. This article is part of the theme issue 'Infectious disease ecology and evolution in a changing world'.

Keywords: adaptation; climate warming; heat shock; heritability; thermal tolerance.

Figure 1.

To test variation in mosquito thermal sensitivity, we submerged glass vials containing mosquitoes in a tank of water heated to 42°C, representing the upper critical thermal limit for the mosquitoes as determined by pilot assay. We then monitored the time it took for mosquitoes to become immobilized, or the ‘knockdown’ (KD) time, using a barcode scanner. For the other half of this design, we heat-shocked mosquitoes from the same families as the aforementioned mosquitoes measured for KD for 15 min at 42°C to induce stress-based expression. We then examined the expression of key heat shock genes (Hsps) in selected families. (Online version in colour.)

Figure 2.

Mean ± s.e. time to knockdown for 40 mosquito families. Heritability was low but significantly different from zero (H² = 0.14, s.e. = 0.09, d.f. = 1, p = 0.028). WT, wildtype. (Online version in colour.)

Figure 3.

Minimum, maximum and mean ± s.e. expression for Hsp 70, Hsp26 and Hsp83 relative to RPS17 for five families each representing (i) a baseline population (no heat-exposed control), (ii) short (fast) KD time families and (iii) long (slow) time to KD families. *p < 0.05, **p < 0.01, ***p < 0.001. (Online version in colour.)