Fertility and mortality impacts of thermal stress from experimental heatwaves on different life stages and their recovery in a model insect

Abstract

With climate change creating a more volatile atmosphere, heatwaves that create thermal stress for living systems will become stronger and more frequent. Using the flour beetle Tribolium castaneum , we measure the impacts of thermal stress from experimental heatwaves in the laboratory on reproduction and survival across different insect life stages, and the extent and pace of any recovery. We exposed larvae, pupae, juvenile and mature adult male beetles to 5-day periods of heat stress where temperatures were maintained at either 40°C or 42°C, a few degrees above the 35°C optimum for this species' population productivity, and then measured survival and reproduction compared with controls at 30°C. Mortality due to thermal stress was greatest among juvenile life stages. Male reproductive function was specifically damaged by high temperatures, especially if experienced through pupal or immature life stages when complete sterility was shown at reproductive maturity; larval exposure did not damage adult male fertility. High temperatures impaired testis development and the production of viable sperm, with damage being strongest when experienced during pupal or juvenile adult stages. Despite this disruption, males recovered from heat stress and, depending on the stage of exposure, testis size, sperm production and fertility returned to normal 15–28 days after exposure. Our experiments reveal how thermal stress from heatwave conditions could impact on insect survival and reproduction across different life stages, and the potential and timescales of recovery.

The mating system affects the temperature sensitivity of male and female fertility

“…Together, these studies suggest that there are several time points with heightened temperature sensitivity throughout male reproductive development. Heat shock treatments applied on adults have also been found to decrease numbers of transferred sperm and reduce fertility (Chevrier et al, 2019;Sales et al, 2018Sales et al, , 2021, but considering the data presented here and in Sales et al (2021), such effects may be reversible in most cases. Similar changes in the morphology of female reproductive organs (i.e., smaller ovaries) combined with a strong reduction in egg number have also been reported for flies of the species Drosophila suzukii developing at elevated temperature (Kirk Green et al, 2019).…”

“…In a later study, the same authors determined the first 20% of larval development to be the most temperature sensitive period of testis development (Vasudeva et al, 2021). A recent study using the flour beetle Tribolium castaneum found that the most sensitive phase of testis development is likely during the pupal stage and that testis size can be almost complete recovered in males exposed to heat stress at an immature adult stage (Sales et al, 2021). Together, these studies suggest that there are several time points with heightened temperature sensitivity throughout male reproductive development.…”

Plastic responses of survival and fertility following heat stress in pupal and adult Drosophila virilis

“…This contrasts with some previous studies that find pupae to be a particularly sensitive life-stage to thermal stress. For example, a recent study examining flour beetles found that pupae and immature males are the most vulnerable life-stages to both fertility loss and survival at high temperatures (Sales, Vasudeva & Gage 2021). Similarly, inD.…”

“…Studies on heat-induced sterility in males typically use either a single long-term stress across age-groups (Rohmer et al 2004;Porcelliet al 2016), or an acute stress to individuals from a single age-group (Jørgensen, Sørensen & Bundgaard 2006;Sales et al2018;Walsh et al 2020;Jørgensen et al 2021). However, it has recently been shown in the flour beetle Tribolium castaneum that the extent of male fertility loss depends on the life-stage exposed to thermal stress (Sales, Vasudeva & Gage 2021). Here, pupal and immature adults show the highest sterility after thermal stress as compared with larval and mature adults.…”

Sperm Production Is Reduced after a Heatwave at the Pupal Stage in the Males of the Parasitoid Wasp Microplitisrufiventris Kok (Hymenoptera; Braconidae)

“…It was shown in Drosophila subobscura that the fertility of males from cold climates was more affected by heat than those from warmer climates [24]. In the flour beetle Tribolium castaneum, the sperm production and viability were reduced after timelimited high temperatures suffered by males [25]. It was shown in some parasitoid wasps (Pteromalidae) that the male sperm production was diminished by heat waves during pupal stages and that the sex ratio of the next generation was strongly male-biased [18,26].…”