Heatwaves are detrimental to fertility in the viviparous tsetse fly.

Heatwaves are increasing in frequency and intensity due to climate change, pushing animals beyond physiological limits. While most studies focus on survival limits, sublethal effects on fertility tend to occur below lethal thresholds, and consequently can be as important for population viability. Typically, male fertility is more heat-sensitive than female fertility, yet direct comparisons are limited. Here, we measured the effect of experimental heatwaves on tsetse flies, Glossina pallidipes, disease vectors and unusual live-bearing insects of sub-Saharan Africa. We exposed males or females to a 3-day heatwave peaking at 36, 38 or 40°C for 2 h, and a 25°C control, monitoring mortality and reproduction over six weeks. For a heatwave peaking at 40°C, mortality was 100%, while a 38°C peak resulted in only 8% acute mortality. Females exposed to the 38°C heatwave experienced a one-week delay in producing offspring, whereas no such delay occurred in males. Over six weeks, heatwaves resulted in equivalent fertility loss in both sexes. Combined with mortality, this lead to a 10% population decline over six weeks compared to the control. Furthermore, parental heatwave exposure gave rise to a female-biased offspring sex ratio. Ultimately, thermal limits of both survival and fertility should be considered when assessing climate change vulnerability.

Systematic approaches to assessing high-temperature limits to fertility in animals.

Critical thermal limits (CTLs) gauge the physiological impact of temperature on survival or critical biological function, aiding predictions of species range shifts and climatic resilience. Two recent Drosophila species studies, using similar approaches to determine temperatures that induce sterility (thermal fertility limits [TFLs]), reveal that TFLs are often lower than CTLs and that TFLs better predict both current species distributions and extinction probability. Moreover, many studies show fertility is more sensitive at less extreme temperatures than survival (thermal sensitivity of fertility [TSF]). These results present a more pessimistic outlook on the consequences of climate change. However, unlike CTLs, TFL data are limited to Drosophila, and variability in TSF methods poses challenges in predicting species responses to increasing temperature. To address these data and methodological gaps, we propose 3 standardized approaches for assessing thermal impacts on fertility. We focus on adult obligate sexual terrestrial invertebrates but also provide modifications for other animal groups and life-history stages. We first outline a "gold-standard" protocol for determining TFLs, focussing on the effects of short-term heat shocks and simulating more frequent extreme heat events predicted by climate models. As this approach may be difficult to apply to some organisms, we then provide a standardized TSF protocol. Finally, we provide a framework to quantify fertility loss in response to extreme heat events in nature, given the limitations in laboratory approaches. Applying these standardized approaches across many taxa, similar to CTLs, will allow robust tests of the impact of fertility loss on species responses to increasing temperatures.

How plastic are upper thermal limits? A comparative study in tsetse (family: Glossinidae) and wider Diptera.

Critical thermal maximum (CTmax) describes the upper thermal tolerance of an animal where biological functions start to fail. A period of acclimation can enhance CTmax through plasticity, potentially buffering animals from extreme temperatures caused by climate change. Basal and acclimated CTmax vary within and between species and may be explained by traits related to thermal physiology, such as body size and sex. Differences in CTmax have not been established among species of tsetse fly (Glossina spp.), vectors of animal and human African trypanosomiasis. Here, we investigated basal CTmax and its plasticity for five tsetse species following adult acclimation at constant 25 or 30 °C for five days. We then set our findings in context using a meta-analysis on 33 species of Diptera. We find that, of the five tsetse species considered, only Glossina palpalis gambiensis and Glossina brevipalpis exhibited plasticity of CTmax, with an increase of 0.12 °C and 0.10 °C per 1 °C acclimation respectively. Within some species, higher basal CTmax values were associated with larger body size and being female, while variation in plasticity (i.e., response to the acclimation temperature) could not be explained by sex or size. Our broader meta-analysis across Diptera revealed overall CTmax plasticity of 0.06 °C per 1 °C acclimation, versus a similar 0.05 °C mean increase in tsetse. In contrast, there was greater CTmax plasticity in males compared to females in Diptera. Our study highlights that CTmax and its plasticity varies even among closely related species. Broader patterns across groups are not always reflected at a finer resolution; we thus emphasise the need for detailed experimental studies across a wide range of insect species to capture their capacity to cope with rapidly warming temperatures.

No evidence for direct thermal carryover effects on starvation tolerance in the obligate blood-feeder, Glossina morsitans morsitans.

Thermal stress during development can prime animals to cope better with similar conditions in later life. Alternatively, negative effects of thermal stress can persist across life stages and result in poorer quality adults (negative carryover effects). As mean temperatures increase due to climate change, evidence for such effects across diverse taxa is required. Using Glossina morsitans morsitans, a species of tsetse fly and vector of trypanosomiasis, we asked whether (i) adaptive developmental plasticity allows flies to survive for longer under food deprivation when pupal and adult temperatures are matched; or (ii) temperature stress during development persists into adulthood, resulting in a greater risk of death. We did not find any advantage of matched pupal and adult temperature in terms of improved starvation tolerance, and no direct negative carryover effects were observed. There was some evidence for indirect carryover effects-high pupal temperature produced flies of lower body mass, which, in turn, resulted in greater starvation risk. However, adult temperature had the largest impact on starvation tolerance by far: flies died 60% faster at 31°C than those experiencing 25°C, consequently reducing survival time from a median of 8 (interquartile range (IQR) 7-9) to 5 (IQR 5-5.25) days. This highlights differences in temperature sensitivity between life stages, as there was no direct effect of pupal temperature on starvation tolerance. Therefore, for some regions of sub-Saharan Africa, climate change may result in a higher mortality rate in emerging tsetse while they search for their first blood meal. This study reinforces existing evidence that responses to temperature are life stage specific and that plasticity may have limited capacity to buffer the effects of climate change.

Meta-analysis reveals weak but pervasive plasticity in insect thermal limits.

Extreme temperature events are increasing in frequency and intensity due to climate change. Such events threaten insects, including pollinators, pests and disease vectors. Insect critical thermal limits can be enhanced through acclimation, yet evidence that plasticity aids survival at extreme temperatures is limited. Here, using meta-analyses across 1374 effect sizes, 74 studies and 102 species, we show that thermal limit plasticity is pervasive but generally weak: per 1 °C rise in acclimation temperature, critical thermal maximum increases by 0.09 °C; and per 1 °C decline, critical thermal minimum decreases by 0.15 °C. Moreover, small but significant publication bias suggests that the magnitude of plasticity is marginally overestimated. We find juvenile insects are more plastic than adults, highlighting that physiological responses of insects vary through ontogeny. Overall, we show critical thermal limit plasticity is likely of limited benefit to insects during extreme climatic events, yet we need more studies in under-represented taxa and geographic regions.