Temperatures that sterilise males better predict global species distributions than lethal temperatures

Abstract

18Climate change is well understood to be a major threat to biodiversity, but sublethal impacts of 19 high temperatures, such as reduced fertility, have been poorly studied. We examined a panel of 20 43 Drosophila species, finding that 19 experience significant fertility loss at temperatures up to 21 4.3 o C cooler than their lethal temperature limits. We found that upper thermal fertility limits 22 explain global distributions of species better than limits based on lethal temperatures. This 23 suggests that limits to reproduction, rather than limits to survival, can underpin species 24 distributions in nature. Given that high temperatures impair male fertility across a broad range of 25 animals and plants, many species may be at increased risk of extinction due to inability to 26 reproduce at high temperatures.27 28 One Sentence Summary: 29 Species' distributions and response to climate change are strongly affected by the temperature at 30 which they lose fertility. 31 3 Main Text: 32 We urgently need to understand how rises in temperature will impact biodiversity(1). To do this 33 we must understand the physiological, behavioral and evolutionary factors that underpin 34 species' current thermal distributions(2, 3). Laboratory-derived estimates of the highest 35 temperatures at which an organism can function provide measures of species' thermal 36 tolerances(4). These measures of upper thermal limits have improved the accuracy of 37 functional species distribution models(5) which can be extrapolated to climate change 38 scenarios, allowing ecologists to forecast future species distributions(6). Accurate predictions of 39 species' distributions are invaluable for prioritizing conservation efforts(7) and predicting the 40 invasion of disease vectors(8). 42Upper thermal tolerance limits are usually based on the temperatures that cause loss of 43 coordinated movement, coma, respiratory failure, or death: the species' critical thermal limit. 44Despite these being measured in artificial laboratory conditions, critical limits correlate 45 reasonably well with species' distributions(4) and have been used to estimate species' capacity 46 to tolerate temperature increases across their current distribution range; their 'thermal safety 47 margins'(3). However, persistence of populations is not determined solely by survival, but also 48 by reproduction. There is evidence that sub-lethal temperatures cause losses in fertility in 49 plants(9), insects(10-12), fish(13), aquatic invertebrates(14), birds(15) and mammals, including 50 humans(16). These effects include direct impacts on physiological processes (10, 15, 17) and 51 indirect influences via changes in behavior and phenology(18). Previously, we proposed that 52 temperatures at which fertility is lost, the thermal fertility limits (TFLs) (18), may be a critical 53 4 but understudied part of species' true upper thermal limits. If TFLs are lower than critical limits, 54 then many organisms will be more vulnerable to climate change than currently thought. If TF...

Age‐specific sensitivity of sperm length and testes size to developmental temperature in the bruchid beetle

“…Alternatively, the effects can result in carry-over effects that negatively impact the adult phenotype, which in turn, can have knock-on effects at higher levels of biological organization (Harrison et al, 2011). The general decline in male fertility in response to thermal stress during development suggests that some of these carry-over effects are negative (O'Connor et al, 2014;Porcelli et al, 2017;Walsh et al, 2019;Parratt et al, 2020). However, in T. castaneum, within generation thermal plasticity in sperm size has been shown to be adaptive: Females mated to experimental males derived from pupae held at either 30 or 38°C produced most offspring, when oviposition took place at the same temperature as that experienced by the male pupae (Vasudeva et al, 2019).…”

“…Alternatively, the effects can result in carry‐over effects that negatively impact the adult phenotype, which in turn, can have knock‐on effects at higher levels of biological organization (Harrison et al ., 2011). The general decline in male fertility in response to thermal stress during development suggests that some of these carry‐over effects are negative (O'Connor et al ., 2014; Porcelli et al ., 2017; Walsh et al ., 2019; Parratt et al ., 2020). However, in T .…”

“…It is becoming increasingly clear that thermal stress impacts fertility (especially of males) before critical lethal temperatures are reached (Walsh et al ., 2019; Parratt et al ., 2020). Recent models indicate that patterns of species distribution are better predicted by thermal fertility limits than lethal temperature limits and that thermal‐fertility limits have important consequences for models of population persistence in the face of global warming (Parratt et al ., 2020). That we show temperature and developmental stage to interact in their effects on the form and function of ‘primary’ reproductive traits.…”

“…However, recently there has been renewed interest in the consequences of sub‐lethal developmental temperature on fertility. Elevated temperatures experienced during development have been shown to reduce both male and female fertility, placing populations at greater risk of extinction in the face of global climate change (David et al ., 2005; Colinet et al, 2015; Sage et al ., 2015; Sales et al ., 2018; Walsh et al ., 2019; Parratt et al ., 2020; Zwoinska et al ., 2020).…”

The genetic basis and adult reproductive consequences of developmental thermal plasticity

“…in the low lines at 29°C. Thus, 29°C for low lines could be taken as close to their thermal fertility limit (Parratt et al, 2021). These reductions correspond to decreases of 15.1% and 73.4% in the fertility of high and low lines, respectively, relative to 25°C (Table 2a; Figure 1b).…”