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

Abstract

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 climate change consequences. However, unlike CTLs, TFL data are limited to Drosophila, and variability in TSF methods pose challenges in predicting species responses to increasing temperature. To address these data and methodological gaps, we propose three standardised 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, focusing on the effects of short-term heat shocks, 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 standardised TSF protocol. Finally, we provide a framework to quantify fertility loss in response to extreme heat events in nature, given limitation in laboratory approaches. Applying these standardised approaches across many taxa, similar to CTLs, will allow robust tests of the impact of fertility loss on species responses to increasing temperatures.

Thermal limits of survival and reproduction depend on stress duration: A case study of Drosophila suzukii

“…Sublethal effects that reduce productivity in individuals are more subtle than direct heat mortality but are essential for delimiting where populations can be maintained. In concordance with recent studies, our work highlights the importance of including thermal fertility limits in assessments of thermal stress vulnerability and in predicting species distributions (Blackburn et al, 2014;Bretman et al, 2024;Green et al, 2019;Iossa, 2019;Parratt et al, 2021;Porcelli et al, 2017;van Heerwaarden & Sgrò, 2021;Walsh et al, 2019).…”

“…However, heat affects the traits differently, and reproduction of D. suzukii was more sensitive than coma and mortality. Studies across a broad range of taxa have similarly identified sublethal effects on reproduction (Bretman et al, 2024;David et al, 2005;Hurley et al, 2018;Parratt et al, 2021;Paxton et al, 2016;Porcelli et al, 2017;van Heerwaarden & Sgrò, 2021), but have largely ignored the important interaction between stress tolerance duration and stress intensity (Cook et al, 2023;Jørgensen et al, 2019Jørgensen et al, , 2021Rezende et al, 2014) as they have typically assessed the loss of fertility in response to a fixed duration of exposure. In this work, we also investigated sterility but have not presented these results as population-level sterility closely followed mortality across all temperatures; that is we could not properly distinguish between heat-induced sterility and mortality with the present experimental setup.…”

“…Irrespective of the trait in question, inclusion of a nuanced time-temperature relationship goes beyond single tolerance metrics, for example CT max (Clusella-Trullas et al, 2021). Especially for species where loss of productivity occurs earlier than mortality during heat stress, inclusion of the time-temperature relationship of both lethal and reproductive limits has the potential to improve predictions of species' vulnerability when combined with relevant information on fluctuations in stress duration and intensity (Bretman et al, 2024;Clusella-Trullas et al, 2021;Parratt et al, 2021;van Heerwaarden & Sgrò, 2021). Such information will be equally important, especially for global pest species such as D. suzukii, when modelling how temperature drives current and future distributions, population dynamics and seasonal phenology (de la Vega & Corley, 2019; dos Santos et al, 2017;Gutierrez et al, 2016;Langille et al, 2017;Maino et al, 2021;Ørsted et al, 2021;Ørsted & Ørsted, 2019).…”

“…Considering the increasing number of studies suggesting that fertility limits may represent better predictors of temperature vulnerability (Bretman et al, 2024;Parratt et al, 2021;van Heerwaarden & Sgrò, 2021), it is of interest to understand if these fertility limits are also characterised by the time-temperature relationship observed for survival and activity traits (Ørsted et al, 2022). Thus, it is possible that discrepancies between the assessment of fertility and coma limits relate to the duration and intensity at which these different traits are measured, and to our knowledge, there has been no work describing how the temperature/duration interaction influences reproductive traits in a manner akin to the TDT model.…”