Cryptic Reproductive Costs of Heatwaves for Animal Populations

ABSTRACT

Heatwaves are among the most serious and immediate threats posed by climate change to biodiversity. While their impacts on mortality are obvious and often severe, heatwaves also have hidden sublethal effects that are only now beginning to be understood. Sublethal effects are particularly significant in reproduction, where heatwaves not only have immediate impacts on fertility and reproductive success, but also trigger transgenerational effects with potential long‐term consequences for populations. Heatwaves impact fitness across all reproductive stages, from gamete formation to offspring production, development, and beyond. These impacts can be cryptic and difficult to observe, potentially extending across generations via parental and epigenetic effects that influence offspring fitness. Crucially, these changes to reproductive phenotypes can then further impact populations by altering sexual selection processes. By increasing variance in reproductive traits, heatwaves can influence both intra‐ and inter‐sexual selection processes and affect pre‐ and post‐copulatory episodes of selection. However, empirical evidence on how heatwaves modulate sexual selection and its evolutionary consequences remains scarce. We argue that identifying and quantifying the cryptic reproductive costs of heatwaves is critical to understanding their impacts on populations at both demographic and evolutionary timescales.

Heatwaves are among the most serious threats posed by climate change to biodiversity. They are known to cause mass mortality events in animals and to strongly affect animal reproduction. The impact of heatwaves on reproduction is crucial because it occurs across all stages, from gamete formation to offspring number and development and beyond. The impacts of heat stress on the parents can extend to the offspring, persist during their whole life, and even transfer across generations. Crucially, by affecting animal reproduction and reproductive traits, such as colorful ornaments, heatwaves can affect sexual selection processes and thus animal populations and evolutionary processes.

1. Introduction

Heatwaves (hereafter HWs), short extreme climatic events where temperatures rise sharply above the seasonal average, are increasing in frequency, intensity, and duration across the globe (Luo et al. 2024). While formal definitions vary, HWs differ markedly from chronic environmental stressors such as pollution or habitat degradation due to their sudden onset and short duration, typically lasting only a few days (Perkins‐Kirkpatrick and Lewis 2020). Nonetheless, projections suggest that HWs' duration will increase exponentially in the coming decades (Martínez‐Villalobos et al. 2025). Their transient nature also makes HWs fundamentally different from gradual warming trends, as they offer little to no time for physiological acclimation. Moreover, HWs involve a rapid and widespread temperature rise that exposes most individuals within a population to the same extreme conditions simultaneously, further distinguishing them from other more heterogeneous environmental stressors. Finally, their interaction with other stressors, whether additive or synergistic, can further complicate and exacerbate their ecological and evolutionary impacts. Thus, understanding HWs' unique mode of action is key to anticipating their influence on population trajectories and resilience in a changing world.

Clearly, despite their short duration, HWs can cause mass mortality events when temperatures exceed the critical thermal limits of organisms, as reported across numerous taxa, including humans (Xu et al. 2016). For example, repeated marine HWs between 2014 and 2016 killed over 4 million common murres ( Uria aalge ), a colonial seabird, representing one of the largest mass mortality events recorded in the modern era (Renner et al. 2024). Given the expected increase in frequency and intensity of HWs in the near future, a large body of current empirical research has understandably focused on assessing mortality thresholds, providing critical insights into organisms' upper thermal limits (Xu et al. 2016). However, focusing exclusively on mortality provides an incomplete picture. Sublethal effects, though often less visible, can profoundly impact populations at many levels, compromising key physiological and ecological processes, such as resistance to parasites, foraging, and metabolism (Martínez‐De León and Thakur 2024). Recent studies have begun to elucidate these HW‐induced sublethal effects across diverse ecosystems and taxa, with most of the evidence to date coming from marine ecosystems (Martínez‐De León and Thakur 2024; Smith et al. 2023; see Table 1). Among sublethal consequences, effects on reproduction are particularly concerning.

TABLE 1.

Overview of heatwave impacts on animal development and condition, phenology, pre‐ and post‐copulatory traits, and transgenerational effects.

Mammals	Birds	Reptiles	Amphibians	Fish	Insects	Arachnids	Crustaceans	Mollusks	Echinoderms
Development and condition
Mouse Mus musculus (lab‐strain) (Olivier et al. 2021)	Great tit Parus major (Bleu et al. 2019), lesser kestrel Falco naumanni (Corregidor‐Castro et al. 2023), Gouldian finch Erythrura gouldiae (Fragueira et al. 2021, 2019)	Common lizard Zootoca vivipara (Brusch et al. 2025), brown anoles Anolis sagrei (Gilbert et al. 2024)	Agile frog Rana dalmatina and European common toad Bufo bufo (Ujszegi et al. 2022)	Pacific cod Gadus macrocephalus (Almeida et al. 2024), zebrafish Danio rerio (Álvarez‐Quintero et al. 2025), three‐spine stickleback Gasterosteus aculeatus (Spence‐Jones et al. 2025)	Damselfly Ischnura elegans (Aramborou et al. 2017), variable field cricket Gryllus lineaticeps (Padda et al. 2021), Drosophila bipectinata (Rashed and Polak 2010)	Mite Amblydromalus limonicus (Walzer et al. 2020)	Copepods Acartia tonsa (Vermandele et al. 2025) and Tigriopus californicus (Siegle et al. 2022); Daphnia magna (Xiao and Wang 2025)	Great pond snail Lymnaea stagnalis (Leicht and Seppälä 2019)	Starfish Parvulastra exigua (Balogh and Byrne 2020), sea urchins: Strongylocentrotus purpuratus (Chamorro et al. 2023), Heliocidaris erythrogramma (Minuti et al. 2022)
Phenology
Richardson's ground squirrel Urocitellus richardsonii (Kucheravy et al. 2021)	Gouldian finch Erythrura gouldiae (Fragueira et al. 2021)				Drosophila virilis (Walsh et al. 2021)		Daphnia magna (Xiao and Wang 2025)
Pre‐copulatory sexual traits
	Zebra finch Taeniopygia guttata (Coomes and Derryberry 2021)			Guppy Poecilia reticulata (Breedveld et al. 2023, 2025)	Seed beetle Callosobruchus maculatus (Baur et al. 2024), red flour beetle Tribolium castaneum (Sales et al. 2018), field cricket Gryllus bimaculatus (Ratz et al. 2024)
Post‐copulatory sexual traits
Mesic four‐striped field mouse Rhabdomys dilectus (Jacobs et al. 2025)	Gouldian finch Erythrura gouldiae (Fragueira et al. 2021), zebra finch Taeniopygia guttata (Hurley et al. 2018), ostrich Struthio camelus (Schou et al. 2021)			Guppy Poecilia reticulata (Breedveld et al. 2023)	Bumblebees Bombus spp. (Martinet et al. 2021), red flour beetle Tribolium castaneum (Moiron et al. 2022; Sales et al. 2018, 2021; Vasudeva et al. 2021), Drosophila virilis (Walsh et al. 2021)			Manila clam Ruditapes philippinarum (Peruzza et al. 2023)	Sea urchin Strongylocentrotus purpuratus (Leach et al. 2021)
Transgenerational effects
				Three‐spine stickleback Gasterosteus aculeatus (Spence‐Jones et al. 2025)	Seed beetle Callosobruchus maculatus (Baur et al. 2024), red flour beetle Tribolium castaneum (Sales et al. 2018)		Brine shrimp Artemia spp. (Norouzitallab et al. 2014), Daphnia magna (Xiao and Wang 2025)		Sea urchins: Strongylocentrotus purpuratus (Chamorro et al. 2023), Heliocidaris erythrogramma (Minuti et al. 2022)

Note: Please note that it is not meant to be an extensive review but rather a summary of representative examples cited in the paper. Animals silhouettes are taken from https://www.phylopic.org/ (CC0 1.0).

Reproduction is highly sensitive to thermal stress, with impacts ranging from impaired gamete production to altered mating behaviors and reduced offspring quality (Walsh et al. 2019). Recent work has revealed that infertility can occur at temperatures well below lethal thermal limits, meaning that population extinctions occur at lower temperatures than expected based on a species' critical thermal maximum (Parratt et al. 2021; van Heerwaarden and Sgrò 2021). This underscores the need to move beyond mortality metrics and explore how HWs affect populations via reproductive disruption. The impacts of HWs on reproduction are important, as HW‐related effects on reproduction can have cascading, far‐reaching consequences for population dynamics and evolutionary trajectories. Moreover, at least in temperate regions, HWs typically occur during the breeding season of most animal species, likely amplifying their impact. Even a single HW event with no apparent effect on adult mortality may substantially reduce population viability if it occurs during this thermally vulnerable life stage. The thermal sensitivity of gametes and embryos (Dahlke et al. 2020), combined with limited abilities to behaviorally thermoregulate in certain breeding organisms, such as nesting birds or aquatic species confined to shallow breeding waters, can further exacerbate the impact of HWs.

Although the effects of HWs on reproduction are sometimes evident, such as failure to reproduce or lower offspring numbers, the reproductive costs of HWs often remain cryptic. This is because, independent of whether fecundity is affected, subtle carry‐over effects on the F1 generation can hinder population viability in the long term. For example, offspring produced during HWs may be in poorer condition, with repercussions ranging from transient to persistent impairments to recruitment and future reproductive success (e.g., effects on F1 survival in adulthood: Pilakouta et al. 2023 and F1 fertility: Spence‐Jones et al. 2025). HWs can also alter parental investment, independent of whether exposure occurs during adulthood or earlier in life, as they can induce long‐lasting changes in individuals. When HWs occur during early life stages, temperature‐dependent developmental and phenotypic plasticity may partly buffer the negative effects of elevated temperature by enhancing short‐term survival (Pottier et al. 2022). However, this initial resilience might come at the cost of altered reproductive phenotype and reduced lifetime fecundity. These individual‐level effects can accumulate across generations, ultimately influencing population dynamics. HW‐induced changes in reproductive traits can further extend beyond fecundity to pre‐ and post‐copulatory traits and may potentially also alter sexual selection processes. Such cascading effects have the potential to shape demography and erode both genetic and phenotypic diversity (Figure 1). Given the potential for these combined hidden effects of HWs to have far‐reaching consequences on populations, it is crucial to explicitly investigate, identify, and quantify their impacts on reproductive processes.

FIGURE 1.

Sublethal effects of heatwaves (HWs) on reproduction can include both obvious, observable, non‐cryptic effects (shown in yellow frames), as well as cryptic effects (shown in grey frames). (A) HW‐induced parental effects can influence offspring quality, with consequences that can persist into adulthood (i.e., carry‐over effects), potentially affecting the offspring's own reproductive output and extending into subsequent generations (i.e., transgenerational effects). (B) When cryptic effects vary among individuals and interact with sexual selection mechanisms, HWs may: (1) alter paternity shares, favoring or disfavouring certain genotypes (illustrated here using differently colored male frogs and their corresponding fertilization success); (2) reduce sire diversity due to male infertility or sub‐fertility, even in polyandrous systems; (3) shift mating systems toward more or less polyandry; and (4) create reproductive bottlenecks, where some genotypes fail entirely to reproduce and disappear from the population, thereby reducing overall genetic diversity. (C) These interacting cryptic effects can ultimately alter demography, reduce genetic and phenotypic diversity, alter heterozygosity, and change the variance in reproductive traits ultimately shaping the population's capacity to persist under environmental change. Created in BioRender: Breedveld, M., Morosinotto, C. (2025) https://BioRender.com/hc55iin.

In this opinion piece, we argue that reproduction is a key interface through which HWs can compromise population persistence, not only via immediate demographic declines but also through subtle, long‐lasting, and transgenerational effects that often go undetected. To capture the full breadth of these reproductive impacts, we first explore the sublethal effects of HWs on reproductive success (Section 2), then examine their cryptic transgenerational consequences and the possible mechanisms involved (Section 3), and finally, discuss how HWs may alter sexual selection dynamics and drive evolutionary changes (Section 4). Through this lens, we aim to reframe how HWs are understood and studied in the context of biodiversity and climate change.

2. Effects of Heatwaves on Reproductive Success

Plastic and condition‐dependent traits, like ornaments, behavioral displays, mating rate, mate choosiness, and sperm production have been shown to be particularly susceptible to HWs (Rashed and Polak 2010; Miwa et al. 2018; Sales et al. 2018; Breedveld et al. 2023; Grandela et al. 2024; Ratz et al. 2024). By affecting these traits, HWs have the potential to compromise reproductive success and negatively affect population demography. HWs may directly impact an individual's ability to find and secure a mate, produce gametes, and/or achieve fertilization, thereby ultimately affecting the number of offspring produced. Alternatively, if experienced during early life stages, HWs can compromise the development of these reproductive traits, with potential repercussions on future reproductive success in adulthood (Figure 2).

FIGURE 2.

Heatwaves (HWs) can affect reproduction through subtle, stage‐dependent mechanisms, with consequences that can extend across generations. This diagram illustrates how HWs may act during different life stages (ontogeny, adulthood, or reproduction) in the parental generation (F0), and how these impacts may extend to subsequent generations (F1, F2…). In the F0 generation, HWs can directly impair reproductive outcomes through impacts on adult traits associated with mate finding, fertility, or parental care. Alternatively, HWs can indirectly compromise reproductive success if their impacts on growth and development have long‐term consequences such as reduced expression of key reproductive traits in adulthood (e.g., competitiveness or attractiveness). Species with parental care represent a special case, as HWs may simultaneously impact both parents and developing embryos or offspring, amplifying cross‐generational effects. Regardless of whether individuals in F0 are stressed during early development or at the time of reproduction, these effects may transfer to the F1 and subsequent generations via transgenerational mechanisms. Created in BioRender: Breedveld, M., Morosinotto, C. (2025) https://BioRender.com/f7f4hke.

HWs can impair mate finding in several ways. Primarily, they may induce changes in the spatio‐temporal distribution of individuals (review in Martínez‐De León and Thakur 2024), potentially causing spatial or temporal (i.e., phenological) mismatches between the sexes, especially when thermal sensitivity is sex‐specific (Iossa 2019). For instance, larval exposure to a HW reduces flight ability in male damselflies (Ischnura elegans), limiting their dispersal and potentially causing a spatial mismatch with receptive females (Arambourou et al. 2017). In Richardson's ground squirrels ( Urocitellus richardsonii ), where males normally emerge from hibernation 8–16 days before females to complete reproductive maturation, a HW led to earlier female emergence, resulting in most males having non‐motile sperm when breeding began (Kucheravy et al. 2021; see Table 1). Sex‐specific thermal sensitivity may also influence sexual size dimorphism (Ketola et al. 2012) or skew sex ratio in species with temperature‐dependent sex determination or sex reversal (Breitenbach et al. 2020; Edmands 2021; Ujszegi et al. 2022; see Section 4).

Gamete production is also highly sensitive to thermal stress across taxa, in species with both internal and external fertilization. HWs can reduce both gamete number and quality, directly impairing fertilization success and causing partial or complete infertility (Parratt et al. 2021; van Heerwaarden and Sgrò 2021). Sperm seem to be particularly sensitive to heat stress (Iossa 2019). For instance, HWs reduce sperm production, viability, or quality in insects (Sales et al. 2018, 2021), sea urchins (Leach et al. 2021), fish (Breedveld et al. 2023), birds (Hurley et al. 2018; Fragueira et al. 2021), and mammals (Jacobs et al. 2025; see Table 1). These changes can affect male competitiveness under sperm competition (when more than one male compete to fertilize the same set of eggs; Parker 1970) and cryptic female choice (when females can bias paternity share among competing males: Eberhard 1996; Firman et al. 2017; see also Figure 1 and Section 4). Female gamete number and quality may also be affected by thermal stress. HW‐induced smaller clutches and overall smaller eggs with different egg composition or structure were indeed observed in clams (Peruzza et al. 2023), sea urchins (Chamorro et al. 2023), fish (Spence‐Jones et al. 2025), reptiles (Gilbert et al. 2024), and birds (Bleu et al. 2019; Wada and Coutts 2021; see Table 1).

HWs can affect reproductive success even when exposure occurs well before the reproductive period if the effects of HWs experienced during early life stages persist into adulthood (Figures 1 and 2). Extreme temperatures during development can compromise growth and condition, potentially leading to long‐term carry‐over effects lasting until adulthood. Short‐term developmental changes due to HWs, such as accelerated development, reduced juvenile size, or changes in condition, have been observed across taxa, including sea urchins (Minuti et al. 2022; Chamorro et al. 2023), crustaceans (Siegle et al. 2022; Vermandele et al. 2025; Xiao and Wang 2025), mites (Walzer et al. 2020), snails (Leicht and Seppälä 2019), starfish (Balogh and Byrne 2020), fish (Álvarez‐Quintero et al. 2025), reptiles (Brusch et al. 2025; Gilbert et al. 2024), birds (Fragueira et al. 2019; Corregidor‐Castro et al. 2023) and mammals (Olivier et al. 2021; see Table 1). Whether these early‐life effects persist until adulthood and affect offspring reproductive output (i.e., transgenerational effects) remains unclear. However, other chronic early‐life stressors, such as predation and food deprivation (Ruell et al. 2013; Vega‐Trejo et al. 2016; Wilson et al. 2019), as well as prolonged elevated temperature (Breckels and Neff 2013; Lee et al. 2014), have been shown to affect sexually selected traits later in life, suggesting that HW‐induced developmental effects may have carry‐over effects on reproductive success.

3. Transgenerational Effects: Offspring Resilience or Offspring Vulnerability?

While most studies on HWs focus on immediate or within‐generation impacts, there is growing evidence that thermal stress can influence not only the exposed individuals but also their offspring (via parental effects) and possibly even subsequent generations (via transgenerational effects). Parental effects can alter offspring phenotype and fitness. These effects are often mediated by the thermal conditions experienced by mothers (maternal effects) and can persist into the adult life of the offspring and affect their own fitness (transgenerational effects), as shown for other stressors such as predation risk (Bhattacharya et al. 2023). Parental effects can also occur through the father; for instance, heat stress on fathers before fertilization can lead to epigenetic changes in the sperm and thereby affect the offspring (e.g., Gasparini et al. 2018; Sales et al. 2018). Parental and transgenerational effects can either buffer or amplify the demographic and evolutionary consequences of HWs.

Parental exposure to HWs can have long‐term carry‐over effects on offspring into adulthood (Baur et al. 2024; Spence‐Jones et al. 2025), which may be detrimental or, in some cases, beneficial. Parental effects can be advantageous when changes to offspring phenotypes enhance survival or performance under future environmental conditions that match those experienced by the parents, as observed in other contexts (Sheriff and Love 2013; Potticary and Duckworth 2020). In three‐spined sticklebacks ( Gasterosteus aculeatus ), adult offspring of HW‐exposed parents had higher survival rates after being themselves exposed to HWs compared to offspring of control parents (Spence‐Jones et al. 2025), suggesting potential transgenerational benefits to F1 survival under matching thermal conditions. Moreover, parental exposure to HWs led to larger clutches but smaller egg size in F1 adult offspring (Spence‐Jones et al. 2025). This effect may be beneficial, as smaller eggs have lower energetic demands in warm water, suggesting that parental experience can help prepare offspring for future environmental conditions. In contrast, in seed beetles (Tribolium maculatus; Baur et al. 2024) and in red flour beetles ( Tribolium castaneum ; Sales et al. 2018), parental exposure to HWs appears to be detrimental, as it has been shown to reduce offspring (F1) fertility. Such detrimental effects on F1 reproductive output were also observed in Daphnia magna, but these HW‐mediated effects disappeared in the following generations (F2–F4) if individuals were not exposed to recurring HWs across generations (Xiao and Wang 2025). Research on chronic heat stress suggests that temperature‐mediated transgenerational effects on body condition and physiology may last up to the third generation (grandparents' effects; spiny chromis damselfish, Acanthochromis polyacanthus ; Bernal et al. 2022; Daphnia magna ; Xiao and Wang 2025). These results suggest that heat‐induced phenotypic shifts and reproductive costs can persist across generations, potentially through non‐genetic inheritance (Bernal et al. 2022; Baur et al. 2024; Spence‐Jones et al. 2025; Xiao and Wang 2025).

Such intergenerational effects have the potential to accumulate over time, leading to additive impacts that could ultimately threaten population viability. In common lizards (Zootoca vivipara), offspring from cold‐adapted populations at high risk of extinction due to global warming are born with shorter telomeres (Dupoué et al. 2022). The authors propose the “aging loop hypothesis,” suggesting that climate warming accelerates physiological aging, resulting in transgenerational accumulation of shortened telomeres. Over time, this could build up across generations, ultimately leading to local extinction (Dupoué et al. 2022). Similar or even more pronounced effects may be expected under repeated HW exposure. Indeed, in humans, an association between heat days and accelerated epigenetic aging has already been observed (Choi and Ailshire 2025). As an unforeseen result, the physiological rate of aging in wild animal populations could thus increase substantially.

While the mechanisms through which HWs could affect multiple generations remain understudied, a plausible process involves epigenetic mechanisms, that is, molecular mechanisms that can alter gene activity without directly altering DNA sequences. Epigenetic mechanisms are increasingly recognized as important mediators of phenotypic plasticity and adaptive potential in the context of climate change in both animals and plants (McCaw et al. 2020; Zetzsche and Fallet 2024; Abdelnour et al. 2024). In line with this, thermal stress has been shown to induce DNA hypermethylation in the gonads and in early embryonic stages of three‐spined sticklebacks, likely affecting sexual development, fertility in adulthood, and phenotypes across generations (Fellous et al. 2022). Changes in sexual traits and gonad development may thus transfer to the germline and have the potential to be inherited (Abdelnour et al. 2024; Fellous et al. 2022). Such epigenetic effects have also been observed to be induced by HWs. For example, in white sturgeons ( Acipenser transmontanus ), juveniles exposed to HWs exhibited increased thermotolerance associated with elevated levels of heat shock proteins (Earhart et al. 2023). While direct evidence of HW‐mediated epigenetic inheritance across multiple generations is still lacking, short and repeated heat stress during development has been shown to cause transgenerational effects in Artemia spp. (Norouzitallab et al. 2014). Unexposed offspring of repeatedly heat‐shocked parents exhibited higher levels of heat shock proteins, increased thermal tolerance, and elevated DNA methylation for up to three generations (Norouzitallab et al. 2014). Although the mechanisms underlying these transgenerational effects remain unclear, existing evidence suggests that HWs, due to their acute intensity and sudden onset, may elicit particularly strong responses. Acute extreme climatic conditions may push species beyond their adaptive thermal thresholds, potentially triggering robust epigenetic responses (Zetzsche and Fallet 2024).

4. Sexual Selection and the Evolutionary Consequences of Cryptic Effects

In Section 2, we discussed how HWs can affect demographic parameters by disrupting traits critical for reproduction. However, HWs may not only shift the population mean of these traits, but also alter their variance, particularly when individuals differ in their sensitivity to thermal stress. Such differential effect can lead to variation in mating and fertilization success, with direct consequences for the strength and direction of sexual selection (Evans and Garcia‐Gonzalez 2016; Figure 3). The opportunity for sexual selection may vary depending on whether HWs increase or reduce phenotypic variance, as observed under other stressors (Cattelan et al. 2020). An increase in variance may amplify differences in competitive ability or attractiveness, potentially intensifying sexual selection. Conversely, reduced variance may mask inter‐individual differences, undermining mate choice and the efficiency of selection. Thereby, HWs could influence intra‐ and inter‐sexual selection processes, affecting pre‐ and post‐copulatory episodes of sexual selection (Figure 3). These dynamics are particularly relevant for plastic and condition‐dependent reproductive traits, which are often highly sensitive to temperature (García‐Roa et al. 2020). As a result, HWs may act not only as demographic stressors, but also as selective filters with the potential to reshape sexual selection mechanisms.

FIGURE 3.

Conceptual diagram highlighting how heatwaves (HW) may affect reproductive traits and sexual selection dynamics, with implications for population resilience. HWs can influence the expression of several reproductive traits, from gametes to ornaments, cognition, and behavioral displays. They can also alter population and operational sex ratios through sex‐specific survival or biased offspring sex ratios. By affecting the expression and especially the variance of pre‐ and post‐copulatory traits, HWs can alter mating and fertilization success variance. These changes shape pre‐ and post‐copulatory sexual selection processes, potentially altering the direction and intensity of selection. Whether these shifts facilitate the evolution of traits that enhance fitness under thermal stress, or instead lead to maladaptive outcomes, will ultimately determine the population's resilience to HWs. Created in BioRender. Breedveld, M., Morosinotto, C. (2025) https://BioRender.com/ovea1gu.

HWs can affect the cost and expression of secondary sexual traits and courtship signals used in mate attraction, mate choice, and competition (Coomes and Derryberry 2021; Martinet et al. 2021; Breedveld et al. 2023; Ratz et al. 2024), with inevitable consequences for pre‐mating sexual selection. In species where access to females is determined by male–male competition and thus depends on traits such as body size or weaponry, HW‐induced changes during development may persist into adulthood and alter dominance hierarchies (Kua et al. 2020; Padda et al. 2021; Ujszegi et al. 2022; Almeida et al. 2024; Goerge and Miles 2024). If HWs reduce males' ability to fully express ornaments due to physiological constraints or increased metabolic costs, trait variability and signal reliability may decline, impairing female discrimination between potential mates. Conversely, if HWs increase trait variance linked to attractiveness, female mate choice should be facilitated and become more effective, potentially intensifying sexual selection and reducing effective population size. If attractiveness is correlated with heritable variation in viability, this could lead to more efficient purging of deleterious mutations, thereby enhancing population resilience (Agrawal 2001; Moiron et al. 2022).

HW‐mediated effects may also directly impact choosers, for example, by impairing their sensory and cognitive capabilities or the time and energy available for mate searching (Rosenthal 2017). Therefore, the impacts of HW‐mediated effects on traits variance through mate choice depend critically on the assumption that mate‐choice mechanisms remain unchanged after thermal stress. However, HWs may disrupt not only the ability to discriminate between potential mates but also the consistency and selectivity of mate choice itself, and in turn, its costs and benefits (Achorn and Rosenthal 2020). Specifically, mate choice involves cognitive properties like attention, memory, and decision‐making (Ryan and Cummings 2013). Studies have shown that HWs can impair cognitive abilities in humans and other animals (Laurent et al. 2018; Danner et al. 2021; Soravia et al. 2021; Breedveld et al. 2025). As a result, thermally induced cognitive impairments could alter female mate choice due to reduced evaluation capacity, potentially exacerbating thermal effects on signal degradation. Interestingly, recent work has demonstrated that HWs can also alter male cognitive performance and mate choice (Breedveld et al. 2025). Since male choice similarly relies on complex cognitive processes, HW‐induced cognitive impairment in both sexes could further shape the direction and strength of pre‐copulatory sexual selection in ways difficult to foresee at this stage.

Post‐mating sexual selection may also be affected by HWs, particularly through their ability to increase among‐male variance in sperm traits. Even when the average level of sperm production or quality is not, or only modestly, reduced, HWs can differentially impact males, with important consequences for post‐mating mechanisms (Figures 1 and 3). For example, some males may remain fully fertile, while others may have reduced sperm quality or even become temporarily sterile, changing completely the ranking of male competitiveness at the post‐mating level. Importantly, some heat‐sterilized males continue to engage in normal sexual behaviors, effectively masking their infertility (Walsh et al. 2021). While females of certain species may detect and avoid sterile males or males with suboptimal fertility (Mak et al. 2023; Grandela et al. 2024), in many cases, females are unlikely to distinguish sterile from fertile males before mating (Vasudeva et al. 2021). This may select for increased female mating rates, that is, polyandry, as a strategy to mitigate fertilization failure (Hasson and Stone 2009; Sutter et al. 2019). Furthermore, by altering the variance in male sperm competitiveness, through effects on sperm quality or quantity, HWs could shift the relative success of competing ejaculates, thus reshaping the outcome of sperm competition and cryptic female choice. Males whose sperm remain functional under thermal stress may gain a disproportionate share of paternity, potentially intensifying post‐copulatory sexual selection (Figure 1).

Sexual selection processes may thus have facilitative, neutral, or detrimental effects on population resilience to HWs (Figure 3). On one hand, sexual selection may facilitate adaptation and population resilience if individuals that are more tolerant to heat stress gain a reproductive advantage, thereby increasing the frequency of beneficial alleles (Cally et al. 2019). For instance, sexual selection can enhance the purging of deleterious mutations when condition‐dependent traits accurately reflect underlying genetic quality (Agrawal 2001). In more extreme cases, sexual selection may hinder adaptation (Candolin and Heuschele 2008). This could occur through antagonistic selection if mate preferences favor traits that are maladaptive under heat stress or if it promotes traits that are costly for females, such as sexual harassment, infanticide, or toxic ejaculates (Chenoweth et al. 2015; García‐Roa et al. 2019). Impaired mate choice may also make it more difficult to find compatible mates, increasing the risk of hybridization or inbreeding. In some cases, sexual selection on males may indirectly favor alleles in females that boost fecundity at the expense of somatic maintenance, an effect that can become detrimental under environmental stress (Chenoweth et al. 2015). Indeed, Baur et al. (2024) showed that females under strong male‐biased selection suffered reduced fecundity when exposed to HWs. Through these mechanisms, sexual selection could thus either buffer or exacerbate the impact of HWs on population viability. Ultimately, the net outcome of HW‐driven shifts in sexual selection will likely be species‐ and context‐specific, depending on mating system, population size, demographic structure, genetic background, and local environmental conditions (Padda et al. 2021; Rowe and Rundle 2021; Leith et al. 2022; Figure 3). Unfortunately, evidence is still limited and concentrated mostly on a few species of insects, birds, and teleost fishes (see Table 1 for some examples). Studies on other groups are needed because the prediction may differ when considering animals with different thermal profiles, physiology, ecological niches, and reproductive systems, such as mammals, reptiles, and non‐insect invertebrates.

HWs may also influence sexual selection and reproductive dynamics by altering the operational sex ratio in natural populations. Changes in the sex ratio can affect key processes such as mate availability, competition, and mate choice. HWs can alter the sex ratio in multiple ways: by inducing sex‐biased mortality, by disrupting temperature‐dependent sex determination during development (Breitenbach et al. 2020), or by triggering sex reversal in thermally sensitive species (Edmands 2021; Ujszegi et al. 2022). For instance, a 6‐day HW during ontogeny caused female‐to‐male sex reversal in agile frogs ( Rana dalmatina ), resulting in a strongly male‐biased sex ratio (Ujszegi et al. 2022). Surprisingly, climate change and HWs could affect the sex ratio also in genotype‐sex determined species. For example, in Gouldian finches (Chloebia gouldia), HW‐exposed mothers produced fewer male offspring than controls, suggesting that the maternal thermal environment can influence sex allocation (Fragueira et al. 2021). Beyond the sex ratio per se, HWs can also reduce female fertility, as demonstrated across taxa (e.g., birds: Schou et al. 2021; fish: Breedveld et al. 2023; insects: Pilakouta et al. 2023). If female fertility is reduced, this yields a restricted pool of reproducing females and a skewed operational sex ratio, leading to higher levels of mate competition and reproductive variance among individuals with downstream effects on sexual selection.

Reproductive dynamics may be further affected through HW‐mediated reduction in genetic diversity. This may occur via drastic reduction in genetic diversity due to mass mortality (Gurgel et al. 2020; Renner et al. 2024). However, HWs may also generate cryptic reproductive bottlenecks, that is, not by killing individuals, but by causing infertility in several individuals, thus restricting reproductive success to a small, often non‐random subset of the population. When only a few individuals contribute genetically to the next generation, the effective population size is reduced (Gurgel et al. 2020; Renner et al. 2024). This hidden, functional reduction in genetic contributors can decrease genetic diversity, increase the risk of inbreeding, and ultimately impair the population's potential for evolutionary adaptation (Figures 1 and 3). Such effects are not limited to males. HWs are likely to affect specific subsets of individuals in sex‐ and trait‐dependent ways. The consequences are expected to be particularly severe in systems where reproduction is already skewed, for instance, in systems where only a few individuals reproduce, such as in demersal fishes where “big old fat females” contribute disproportionately to recruitment (Hixon et al. 2014). If a HW disproportionately impacts these rare but crucial breeders, population viability may collapse despite other seemingly stable demographic metrics.

Altogether, empirical evidence suggests that HWs are an increasingly pivotal player in the evolutionary interplay between thermal ecology and sexual selection (Leith et al. 2022). Yet, most experimental studies have focused on how environmental stress affects the average expression of male and female traits or mean reproductive success (typically by comparing control and stressed individuals; e.g., in a heat stress context: Martinet et al. 2021; Vasudeva et al. 2021; Moiron et al. 2022). However, given the interactive nature of sexual selection (Evans and Garcia‐Gonzalez 2016) and given that heat stress likely affects both sexes simultaneously, we encourage a shift in experimental focus. Specifically, we must go beyond mean effects and examine how HWs alter variance in sexually selected traits and reproductive success, since it is variance, not mean values, that underpins the opportunity for sexual selection. Understanding how HWs reshape the distribution of reproductive outcomes is essential to predict their role in evolutionary processes.

5. Conclusions

HWs represent transient yet severe stressors that affect entire populations simultaneously. Although frequent intense HWs may eventually drive the evolution of thermal tolerance, mounting evidence suggests that their sublethal impacts on reproduction could be detrimental to populations. These sublethal effects, often cryptic, could play a key role in determining individual and population‐level sensitivity to HWs. However, they remain poorly understood and are rarely incorporated into current ecological or evolutionary models predicting population responses to climate change.

Here, we discussed several pathways through which HWs could affect reproduction and the potential consequences on populations. Among these, a reduction in effective population size (and hence genetic variability) due to HW‐induced male infertility seems particularly worrying for population viability. Similarly, HW‐induced transgenerational effects are likely to have important consequences for populations, especially under repeated HW exposure that may lead to cumulative effects across generations. Finally, HWs are expected to interact with sexual selection processes in complex ways, potentially altering mate choice dynamics and reproductive success. The net effect of HWs on reproduction and population fitness remains difficult to predict and is likely to be context‐dependent. It will inevitably vary across species and life stages, depending on factors such as mating system, reproductive mode, and the extent of parental care as well as the thermal ecology of a species.

While current evidence points to consistent trends across studied organisms, future research should include a broader range of taxonomic groups to provide a more comprehensive assessment of HW impacts on biodiversity. To more accurately assess reproduction's role as a mediator of individual and population‐level sensitivity to HWs, targeted experimental and theoretical work is essential. These studies should examine how short‐term thermal extremes affect reproductive function, fitness variance, and genetic diversity—while accounting for variation in mating systems—to understand HWs' effects on sexual selection and evolutionary dynamics in exposed populations. At the same time, it is crucial to monitor responses across multiple generations and investigate potential mechanisms of epigenetic inheritance, as the effects of repeated HWs may accumulate over time. Ideally, using standardized experimental approaches across multiple species, or among different populations across a species' geographical range, could help to disentangle the mechanisms underlying HW‐mediated effects. In a world where climate warming and HW intensity are accelerating, understanding the complex interplay between HWs and reproduction is not just a theoretical challenge; it is essential for predicting species persistence and informing conservation strategies in a rapidly changing environment.

Author Contributions

Chiara Morosinotto: conceptualization, funding acquisition, visualization, writing – original draft, writing – review and editing. Clelia Gasparini: conceptualization, funding acquisition, writing – original draft, writing – review and editing. Andrea Pilastro: conceptualization, funding acquisition, writing – original draft, writing – review and editing. Gil Guastoni Rosenthal: conceptualization, funding acquisition, writing – review and editing. Merel C. Breedveld: conceptualization, funding acquisition, visualization, writing – original draft, writing – review and editing.

Conflicts of Interest

The authors declare no conflicts of interest.

Morosinotto, C. , Gasparini C., Pilastro A., Rosenthal G. G., and Breedveld M. C.. 2025. “Cryptic Reproductive Costs of Heatwaves for Animal Populations.” Global Change Biology 31, no. 11: e70558. 10.1111/gcb.70558.

Data Availability Statement

Data sharing is not applicable to this article as no datasets were generated or analysed during the current study.