Male fertility thermal limits predict vulnerability to climate warming

Projected increases in average temperature, as well as the frequency and duration of extreme heat events and heat waves, pose a major risk to species persistence and biodiversity. Understanding and predicting how species will respond to climate change and identifying which species are most vulnerable will be paramount to successfully managing biodiversity. Trait-based approaches (which compare estimates of thermal tolerance or performance to current and future habitat temperatures to calculate species’ thermal safety margins or warming tolerance) have been utilized to examine vulnerability across different latitudes and habitats. These studies suggest that tropical and mid-latitude species—which make up the vast majority of the world’s biodiversity—are predicted to be most vulnerable because they already experience maximum habitat temperatures close to their upper thermal limits. However, these studies have predominantly focused on upper critical thermal limits (CTLs), the temperature at which adults stop moving or die, assuming that acute heat tolerance will be important in determining species’ vulnerability to future climate change. This is largely driven by data that suggest that upper CTLs are better predictors of current distributions than other fitness measures, like optimum performance temperature (Topt). Nonetheless, associations between upper CTLs and species’ distributions or abundance are often weak or absent, questioning the capacity for CTLs to predict future distributions under climate change. Significantly, emerging data suggest that upper CTLs—which are typically estimated on adults—may underestimate species’ climate vulnerability. Data from a recent comparative study on fish found that spawning adults and embryos have narrower thermal tolerance ranges than non-reproductive active adults or larvae. There is also growing evidence suggesting that ectotherms, especially male ectotherms, may become sterile at temperatures much below their lethal (critical) thermal limits. These studies suggest that upper CTLs using adults may underestimate vulnerability, yet explicit tests of whether other measures of thermal tolerance—such as fertility thermal limits (FTLs)—are better predictors of vulnerability to climate change are currently lacking. Trait-based approaches to assessing vulnerability also largely ignore the extent to which adaptive responses (genetic evolution and phenotypic plasticity) may ameliorate the negative impacts of climate change. This is despite the fact that adaptive responses may play a crucial role in species persistence and evolutionary rescue and an increasing number of studies show that evolution and plasticity contribute to recent climate change responses in the wild. Recent studies suggest that species, particularly those in the tropics, may have a limited capacity to increase upper CTLs via evolutionary or plastic shifts. Yet, most studies on adaptive responses to increased temperatures have been performed under environmental conditions that bear little resemblance to conditions encountered by natural populations. This is significant because additive genetic variance (the genetic variance that underpins heritability and adaptive capacity) may change under different environmental conditions. Whether adaptive evolutionary responses to climate warming, using ecologically relevant temperature fluctuations, are limited across tropical and widespread species is unclear. Furthermore, the extent to which other measures of thermal tolerance—such as male FTLs, which may underpin vulnerability to climate change—are able to evolve in response to climate warming is unknown.

Previous research has indicated that tropical and mid-latitude species are particularly vulnerable to climate warming due to their proximity to their upper thermal limits. Studies using trait-based approaches, often focusing on upper critical thermal limits (CTLs), suggested a strong correlation between CTLs and species distributions. However, these correlations have been inconsistent, raising doubts about the accuracy of CTLs as predictors of vulnerability. Furthermore, existing research has largely overlooked the role of adaptive responses (evolutionary and plastic changes) in mitigating the impacts of climate warming. Some studies suggest limited capacity for increasing upper CTLs through evolution or plasticity in tropical species. However, many of these studies used unrealistic experimental conditions, lacking the ecological relevance of natural temperature fluctuations. The importance of fertility thermal limits (FTLs), specifically in males, as potential predictors of climate change vulnerability was largely unexplored.

This study used experimental evolution to investigate the extinction risk and adaptive responses of six Drosophila species (three tropical, three widespread) to warming. The experiment employed a fluctuating temperature regime mimicking natural summer temperatures in tropical Australia, gradually increasing the average temperature over time. The researchers monitored population persistence, measuring the temperature at which extinction occurred. They assessed various thermal traits, including upper CTLs (CTmax), developmental male and female upper FTLs, and pre-adult viability thermal limits (VTLs). These traits were measured using fluctuating thermal regimes during development, extracting LT50 and LT80 estimates. Published Topt estimates were also incorporated where available. The relationship between these thermal traits and extinction temperature was analyzed using linear regressions. To assess the potential for adaptation, the researchers compared male fertility, male sterility, and CTmax in control and selected lines after various levels of warming, under both control and selected developmental temperatures. The effects of selection and developmental temperature were analyzed using generalized linear mixed models. Finally, the study examined the association between male FTL50, CTmax, and Topt with climatic variables across a broader set of ten species, and calculated warming tolerances and thermal safety margins based on the different thermal limits to assess how closely the species were living to their thermal limits.

The study found that tropical Drosophila species went extinct at significantly lower temperatures than widespread species under experimental warming. Male upper FTL50 estimates proved to be better predictors of extinction risk and species distributions than CTmax. The average extinction temperature was closely matched by male FTL50, whereas CTmax significantly overestimated extinction temperatures. There was little evidence for adaptive evolutionary responses to warming in any species for either male sterility/fertility or CTmax. Adaptive developmental plasticity was also limited, showing minimal increases in CTmax in response to warming. The thermal safety margins based on male FTL50 were considerably lower than those calculated using CTmax, suggesting that current assessments using CTmax substantially underestimate individual species' climate change risk. Tropical species displayed thermal safety margins using male FTL50 often below two degrees, indicating their proximity to their reproductive limits. While both warming tolerance and thermal safety margins using different traits showed associations with latitude, safety margins based on male FTL50 provided a more accurate reflection of individual risk, particularly in tropical species.

The findings challenge the prevailing assumption that upper CTLs accurately predict climate change vulnerability. The strong correlation between male FTL50 and extinction temperatures, coupled with its superior predictive power compared to CTmax, highlights the importance of male fertility in determining species' responses to warming. The lack of adaptive responses (evolutionary and plastic) suggests limited capacity for species to cope with projected temperature increases. Tropical species, already living close to their reproductive thermal limits, appear especially vulnerable. The study's results underscore the need to incorporate FTLs, particularly male FTLs, into climate change vulnerability assessments. The use of ecologically relevant temperature fluctuations in the experimental design strengthens the relevance of the findings to natural populations.

This study demonstrates that male fertility thermal limits are crucial determinants of extinction risk under climate warming, providing a more accurate predictor than previously used measures like CTmax. The limited capacity for adaptive responses, both evolutionary and plastic, highlights the significant vulnerability of many species, especially those in the tropics. Future research should further investigate the impact of sub-fertility and extreme temperature events on population persistence and explore the potential role of transgenerational plasticity. Incorporating FTLs into climate change vulnerability assessments is critical for effective conservation strategies.

The study's experimental warming regime, while ecologically relevant, may not perfectly capture the natural complexities of seasonal and microclimate temperature variations. The focus on complete sterility might underestimate the effects of climate change, as reductions in male fertility (sub-fertility) can also negatively impact population persistence. The study did not explicitly consider interactions between extreme temperatures and above-average developmental temperatures, which might further affect fertility. The limited number of species and replicate lines used might limit the generalizability of the findings to other taxa.