Trade-offs between Winter Survival and Reproduction in Female Insects

Synopsis

In temperate environments, most species of insects enter an arrested state of development, known as diapause, that enables them to survive the adverse environmental conditions associated with winter. Although diapause is restricted to a single life stage within species of insects, there are examples of insects that overwinter in the egg, larval, pupal, and adult stages. Here we offer a targeted, non-systematic literature review examining how overwintering impacts subsequent reproduction in female insects. Several factors, including the lifestage at which insects overwinter, the type of energy investment strategy females use for breeding, elements of the winter environment, and contributions from male insects can influence trade-offs that female insects face between overwintering survival and post-diapause reproduction. Additionally, climate change and elements of the urban environment, including light pollution and higher temperatures in cities, can exacerbate or ameliorate trade-offs faced by reproducing female insects. Better understanding the trade-offs between overwintering survival and reproduction in insects not only enhances our understanding of the underlying physiological mechanisms and ecological processes governing diapause and reproduction, but also provides opportunities to better manage insect pests and/or support beneficial insects.

Introduction

Unlike birds and mammals, most female insects are R-strategists and therefore do not substantially invest in maternal care. However, some insect species (including some male insects) exhibit post-zygotic care and maternal care is widely distributed across class Insecta (reviewed by Tallamy and Brown 1999). Yet, even for the majority of insects that do not care for their young, reproducing female insects face trade-offs between the number of eggs and the size of eggs that they can produce, and female reproduction is strongly influenced by the environment (reviewed by Labeyrie 1978).

Temperate insects face additional challenges because, as ectotherms, they must engage physiological and behavioral mechanisms that allow them to survive low temperatures and the absence of food during winter. Diapause is a physiologically dynamic state of arrested development that allows insects to survive inimical seasons (reviewed by Denlinger 2022). However, entering diapause is energetically expensive, requiring careful use of energy stores (reviewed by Hahn and Denlinger 2007, 2011; Roberts et al. 2023b). It therefore seems likely that insects investing energy in overwintering survival may encounter reproductive trade-offs. As female insects invest greater energy in gamete production relative to males (Hayward and Gillooly 2011), it also seems likely that females that successfully overwinter will experience greater fitness trade-offs than males.

Here we offer a targeted and nonsystematic review of the literature that examines the interplay between the environment, diapause, and reproduction in insects (Fig. 1). We first explore the extent to which the developmental stage when insects overwinter impacts fecundity and/or lifetime fitness. Second, we explore how elements of the overwintering environment, such as temperature extremes and diapause duration, affect reproductive trade-offs in females relative to males. We then examine evidence suggesting that male insects can help females overcome the trade-offs associated with overwintering by modifying the composition of their ejaculate to enhance female immune function and/or fecundity. Finally, we discuss how human-mediated changes to the environment, such as climate change, light pollution, and urban heat islands (UHIs), have the potential to exacerbate and/or ameliorate the trade-offs faced by reproducing females.

Fig. 1.

Multiple factors affect the trade-offs that female insects face between overwintering survival/diapause and reproduction. These include the species-specific stage at which females overwinter, the source of energy that they use for reproduction (e.g., capital vs. income breeders), and elements of the winter environment. It is also possible that male insects can influence trade-offs between reproduction and survival in post-diapause females, and that climate change and urbanization have the potential to ameliorate or exacerbate trade-offs (see text for details). Eggs were drawn by M. Meuti. All other icons were obtained from the Noun Project.

Sex and stage specific trade-offs between diapause and reproduction

In multivoltine insect populations (those that produce multiple generations each year), most individuals do not need to survive the winter. Only the late summer and early autumn portions of the population need to confront winter by entering diapause. The capacity for diapause is usually restricted to a single life stage (reviewed by Denlinger 2002, 2022), but there are examples of insects that overwinter in the egg, larval/nymphal, pupal, and adult stages. Separating the costs of entering diapause from stresses in the overwintering environment, as well as determining the impact of diapause on post-diapause reproduction is experimentally challenging (reviewed by Denlinger 2022). Though the literature examining diapause costs is rather limited, several studies have demonstrated the impact of overwintering diapause on the reproductive performance of female insects.

Reproductive trade-offs associated with embryonic diapause

It is currently unclear how undergoing an embryonic diapause impacts the fecundity of the adult females later in life. One might anticipate that the stress of having survived the winter as an embryo would reduce fecundity in females. Notably, however, this need not be the case, as the intervening larval stages could enable the female to garner the requisite energy reserves to successfully reproduce. Additionally, exiting diapause at the proper time in spring would also allow developing insects to appropriately coordinate their emergence with food availability, and potentially enhance their reproductive potential. Interestingly, exephippial generations of Daphnia that successfully overwinter matured faster, are larger, and significantly more fecund than directly developing parthenogenic females (Arbačiauskas and Gasiūnaitė 1996), demonstrating that arresting embryonic development has the potential to enhance female reproduction and allow populations to rapidly increase in the spring.

But, as females must produce eggs that have to successfully overwinter, and these eggs are, in some cases, larger and have greater nutrient reserves, it is also likely that the maternal insects that lay diapausing eggs are less fecund than those that lay non-diapausing eggs. Indeed, this is true in the American rock pool mosquito, Aedes altropalpus, and the tiger mosquito, Ae. albopictus, where females produce higher numbers of smaller, non-diapausing eggs when exposed to long-day, summer-like conditions relative to females that are exposed to short-day, winter-like conditions (Kalpage and Brust 1974; Lacour et al. 2014). There are also several examples where female insects lay increasing proportions of diapausing eggs as they age (Saunders 1962; Ring 1967; McNeil and Rabb 1973; Rockey and Denlinger 1986; Hockham et al. 2001). This makes ecological sense, as the older the female is, the more likely it is for winter to arrive and the less time her offspring would have to reach reproductive maturity before winter’s onset. However, changing the proportion of diapausing eggs may also allow females to compensate for trade-offs by producing high numbers of smaller, non-diapausing eggs earlier in life and then lower numbers of larger, diapausing eggs later.

Reproductive costs of diapause in immature stages

Overwintering as an immature insect or as a pre-reproductive adult has obvious advantages in that such insects are typically able to acquire more nutrient reserves before entering their overwintering dormancy. Additionally, if the insects overwinter as mobile larvae, nymphs, or pre-reproductive adults, they are able to move to a suitable overwintering site, or hibernacula. Although pupae are immobile, they can garner sufficient nutrient reserves as larvae and can move to their preferred hibernacula before pupation (reviewed by Denlinger 2022). Both males and females of many species diapause in the immature stage, including in Lepidoptera, where larval diapauses are the most common (Halali et al. 2024), and in some species, females experience greater fitness consequences.

Bradshaw et al. (1998) found that larvae of the pitcher plant mosquito, Wyeomia smithii, subjected to overwintering conditions in the laboratory suffered a 60% loss in fitness relative to larvae that had been maintained under optimal summer conditions. Reductions in fitness were because of both lower survivorship and a significantly lower mass-specific fecundity, despite that overwintered mosquitoes pupated and matured as adults under the same conditions as those that were reared under optimal conditions. These results underscore that the decrease in female fecundity is reflective of the latent cost of overwintering (Bradshaw et al. 1998). Notably, in this study, both male and female larvae had overwintered and were allowed to mate with each other, making it difficult to determine the extent to which the decrease in fecundity was derived from female-specific (e.g., lower nutrient reserves for vitellogenesis and egg production) or male-specific (e.g., lower quality ejaculate and/or fewer sperm transferred) effects.

Several studies have examined sex-specific differences on the impact of overwintering during immature life stages on subsequent reproduction in males and females. For example, fruit moths, Grapholita funebrana, and codling moths, Cydia pomonella, that undergo a pre-pupal overwintering diapause produce fewer offspring as adults, which is due to both lower rates of oviposition and mating (Deseo 1973). Additionally, post-diapause males of C. pomonella have a smaller testicular size, suggesting that both sexes may suffer from post-diapause reproductive trade-offs. Males and females of another lepidopteran pest, the spotted stem borer (Chilo partellus), suffer reduced fecundity after diapausing in the larval stage (Dhillon and Hasan 2018). Similarly, reciprocal crosses of post-diapausing and non-diapausing males and females of the bruchid beetle, Acanthoscelides pallidipennis, revealed that both post-diapause females and non-diapausing females that mated to post-diapause males took longer to oviposit and laid fewer eggs than those that had mated with non-diapausing males (Sadakiyo and Ishihara 2012).

In other insect species that overwinter in immature stages, post-diapause female insects suffer a fitness cost while males do not. Specifically, Win and Ishikawa (2015) demonstrated that although post-diapause males of the adzuki bean borer, Ostrinia scapulalis, were smaller and had lower levels of mating success than their non-diapausing counterparts, post-diapause males transferred similar levels of sperm. Additionally, non-diapausing females mated with post-diapause males of O. scapulalis produced similar numbers of eggs as those that had mated with non-diapausing males (Win and Ishikawa 2015). Taken together, these results demonstrate that males of this species do not face reproductive trade-offs after overwintering.

Notably, Denlinger (1981) demonstrated that females of the flesh fly, Sarcophaga crassipalpis, that overwintered as diapausing pupae produced fewer offspring regardless of whether they mated with a male of non-diapause or diapause history, a cost that increased with the duration of the female’s diapause. In contrast, males that had overwintered were able to sire as many offspring as males that had not undergone diapause when they mated with a female with a non-diapause history (Denlinger 1981). This female-specific decrease in fecundity following diapause termination underscores the trade-offs that many female insects face between allocating energetic resources towards overwintering survival and future reproduction. It can also further explain sex-specific differences in timing of diapause initiation in the field; male insects of many species enter diapause earlier in the season than females (Ring 1971; Denlinger 1972; Kaldeh et al. 2018). A likely explanation is that males do not face the same reproductive trade-offs as females, but further research is necessary to verify whether this is indeed the case.

A novel type of trade-off is noted in the pipevine swallowtail, Battus philenor (Fordyce et al. 2006). Females that emerge following pupal diapause contain less fat than their nondiapausing counterparts, a fitness correlate that suggests they would be able to produce fewer eggs. However, post-diapause female B. philenor are better defended with larger deposits of aristolochic acid, a chemical defense they acquire from their larval host plants. An example such as this suggests the layers of complexity that may be involved in calculating costs and benefits of diapause.

Reproductive costs of diapause in adult males

In numerous species, both males and females overwinter in diapause, and in these cases, males typically do not mature their reproductive organs or mate with females until after terminating diapause (reviewed by Pener 1992). However, this is not universal: there are several species where mating can occur both before and after diapause (Awad et al. 2013; Konagaya and Watanabe 2015). Reproductive trade-offs in post-diapause males could include reduction in number of total copulations or copulation frequency, reduced mating duration, lower-quality or quantity ejaculate, and/or a reduction in the number of sperm transferred, each of which could result in a decrease in the number of total offspring that post-diapause males would be able to produce.

Mating performance and fitness consequences in males that enter dormancy as adults have been measured in a few insect species. Notably, Kubrak et al. (2016) found that females of Drosophila melanogaster that mated with males that had recovered from dormancy produced significantly fewer offspring relative to those that had mated with non-dormant males. In a closely related species, D. montana, post-diapause males also initially showed lower mating performance and reproductive success, but after being exposed to diapause-terminating conditions for four days, male D. montana were able to stimulate similar levels of egg laying and offspring production in non-diapausing females (Ala-Honkola et al. 2020). Additionally, post-diapausing males were able to father the same number of offspring as males without a diapause history when mated to post-diapause females.

In some species, male insects that enter diapause may not incur a reproductive cost. For example, in the Asian comma butterfly, Polygonia c-auruem, both summer and autumnal, pre-diapausing males engaged in similar levels of spermatogenesis early in adult life (Hiroyoshi et al. 2020), suggesting that these males might not experience a trade-off between overwintering and reproduction. However, additional studies are necessary to determine whether post-diapause males are as virile as non-diapausing males.

Currently, it is unclear why males of some insects that overwinter as adults experience fitness trade-offs and others do not. Some of these discrepancies could potentially be explained by differences in when and how male insects acquire the energetic reserves for spermatogenesis, seminal fluid production, and mating. For example, males that rely on energetic reserves they acquired at earlier life stages (so-called “capital breeders”) would be more likely to face reproductive consequences upon terminating dormancy due to depletion of these reserves. Alternatively, males that utilize energy acquired after diapause termination (“income breeders”) would be able to compensate for any nutrient depletion and hence would be less likely to face reproductive trade-offs (modeled by Varpe and Ejsmond 2018; reviewed by Denlinger 2022).

Reproductive costs of diapause in adult females

As seen in adult males that overwinter in diapause, diapausing adult females must invest precious energy resources into overwintering survival, resulting in lower body weight, and thus have less energy for investing in reproduction (reviewed by Pener 1992). Therefore, it is not surprising that post-diapause females of the nymphalid butterfly P. c-aureum, the adzuki bean borer (O. scapulalis), and the grasshopper Stenocatantops splendens produce fewer eggs than non-diapausing females (Zhu et al. 2013; Win and Ishikawa 2015; Hiroyoshi et al. 2020). Females of the bruchid A. pallidipennis reared in diapausing conditions are also smaller and produce fewer eggs than their nondiapausing counterparts (Sadakiyo and Ishihara 2012).

In some other insect species, only adult females are capable of entering diapause, and thus females must mate in the fall and successfully store and maintain the sperm throughout the entire duration of winter. Post-diapause females of these species might experience a greater energetic cost to maintain the sperm and therefore face larger reproductive trade-offs. Determining the exact costs of sperm maintenance and survival is complicated, however, as it would require measuring differences in the reproductive output of females that have mated before and after diapause termination, and this would be limited to a few species where mating can occur in either the fall or spring. However, females of the ladybird beetle H. axyridis that had mated before diapause began laying eggs sooner and laid more eggs than virgin, post-diapause females (Awad et al. 2013). In this case, there appears to be no cost to females that mate before diapause entry. However, it would be interesting to measure the reproductive performance of post-diapause females that mated after diapause termination to determine whether post-diapause females that mated more recently would initiate oviposition and produce similar numbers of eggs as females that mated before initiating diapause.

To determine whether post-diapause females of the Northern house mosquito, Culex pipiens, face reproductive tradeoffs, we compared the reproductive output of non-diapausing and post-diapausing females (Fig. 2). In this species, nearly all females mate before entering diapause (Onyeka and Boreham 1987) and rely on the sperm they receive in the fall to produce viable offspring the following spring. In comparing the number of larvae that females produced from their first clutch of eggs, we found that individual post-diapausing females produced on average 35% fewer larvae than non-diapausing females (P = 0.0195; Fig. 2). Future studies should examine whether there is a differential reproductive output that carries into subsequent gonotrophic cycles. Additionally, differences in the metabolic rate of mated and virgin diapausing females may help reveal the energetic costs of sperm maintenance.

Fig. 2.

Surviving diapause is associated with a decrease in fertility in female Northern house mosquitoes. Circles represent the total number of larvae in the first clutch of eggs laid by individual female Culex pipiens; lines represent the average number of offspring per female. * indicates a statistically significant difference (student’s T-test; P = 0.0195). Original data collected and analyzed for this review article.

There are notable exceptions where post-diapause females do not experience a decrease in fecundity or may in fact produce more offspring than non-diapausing females. For example, non-diapause and post-diapause females of the green stink bug, Nezara viridula, have a similar duration of oviposition and produce similar numbers of offspring (Musolin et al. 2007), while females of the cabbage beetle, Colaphellus bowringi that have experienced a prolonged diapause are more fecund than non-diapausing females, and their offspring develop faster (Wang et al. 2006). Differences in the energetic investment strategy for reproduction (e.g., differences between income and capital breeders) along with differences in adult body size can likely explain why females of some insect species are able to avoid trade-offs between overwintering survival and subsequent reproduction (reviewed by Denlinger 2022).

Elements of the overwintering environment that impact reproductive trade-offs

In addition to the life stage at which insects overwinter, elements of the overwintering environment itself also impose reproductive trade-offs for male and especially female insects. As environmental conditions become more extreme and/or food becomes more limited, female insects must invest more energy into winter survival and therefore have less resources available for subsequent reproduction (reviewed by Leather 1995). Specifically, temperature, food quality, and diapause duration impact the energy reserves and subsequent reproductive performance of female insects, and many studies indicate that females experience greater decreases in fecundity relative to males.

Both high and low temperatures during winter can adversely impact survival and thus female fitness (reviewed by Williams et al. 2015; Marshall et al. 2020). At low temperatures, insects must invest energy in cryoprotection and/or repairing cellular damage from freezing (Marshall and Sinclair 2011, 2015; Štětina et al. 2018; Koštál et al. 2019). The diapause program itself may allow insects to ameliorate these costs. For example, although both diapausing and quiescent pupae of the apple maggot fly, Rhagoletis pomonella, exhibit similar tolerance to an extreme low temperature (−18°C) after a period of cold acclimation, significantly fewer quiescent insects survive prolonged periods of cold exposure (eight or more weeks held at 4°C) relative to diapausing pupae (Toxopeus et al. 2021). A cold, dry environment devoid of snow delays the upregulation of reproductive processes in the willow leaf beetle, Chysomela aeneicallis (Roberts et al. 2023a); thus, how long an insect remains dormant is highly dependent on diverse features of the environment.

On the other hand, high overwintering temperatures are also stressful for diapausing insects because they elevate metabolic rates, causing rapid depletion of nutrient reserves. For example, Lehmann et al. (2015) demonstrated that increasing temperature elevates metabolic rate in four different populations of diapausing Colorado potato beetles. Diapausing pupae of the fall webworm, Hyphantria cunea, held at high temperatures weigh less and deplete carbohydrate and protein reserves more rapidly than those held at lower temperatures, yet in this species lipid levels and survival are not affected (Zhao and Wang 2021). High winter temperatures reduce overwintering survival of diapausing pupae of the Baltimore checkerspot butterfly, Euphydryas phaeton phaeton (Abarca et al. 2019), and larvae of the green-veined white butterfly, Pieris napi (Nielsen et al. 2022). Additionally, high winter temperatures reduce both survival of diapausing larvae of the goldenrod gall fly, Eurosta solidaginis, and potential post-diapause fecundity of females (e.g., lower numbers of eggs in the ovaries), whereas low overwintering temperatures have a protective effect (Irwin and Lee 2000, 2003). Similarly, adult females of the rose-galling wasp, Diplopesis spinosa, exposed to 10°C as diapausing prepupae produce 32% fewer eggs than those held at 0°C (Williams et al. 2003). High temperatures, in combination with deforestation, also reduce overwintering survival and lipid reserves of non-reproductive females of the Scottish wood ant, Formica aquilonia (Sorvari et al. 2011).

Given the interplay between temperature, metabolism, and the energetic reserves required to survive winter and subsequently reproduce, it is not surprising that diet can also substantially impact the fitness of female insects (reviewed by Short and Hahn 2023). Survival and fecundity of female lady beetles of H. axyridis are positively correlated with food quality, regardless of the photoperiodic cues (Reznik and Vaghina 2013). Notably, although high overwintering temperatures do not impact the overwintering survival or the egg-laying ability of post-diapause queens of the white-tailed bumble bee, Bombus terrestris, overwintering survival is dependent on female weight, such that no females weighing less than 0.6 g are able to survive the winter (Beekman et al. 1998).

Diapause duration can also significantly impact insect survival and fecundity, and in some species, females appear to be more affected than males. In the solitary ground nesting bee, Osmia lignaria, pre-wintering duration is negatively correlated with weight, lipid levels, and female post-winter longevity (Bosch and Kemp 2000; Bosch et al. 2010; Sgolastra et al. 2011). However, pre-winter duration does not impact nesting duration, fecundity, or parental investment (e.g., weight of pollen and nectar that females provided to each larva), likely because post-diapause female O. lignaria exhibits an income breeding strategy by taking advantage of abundant food resources to replenish their nutrient reserves and those of their offspring (Sgolastra et al. 2016). Diapuase duration in emerald ash borers, ranging from 2 to 9 months, does not significantly impact longevity or the lifetime fecundity of females, suggesting that members of this species are also likely income breeders (Duan et al. 2021). In contrast, females of the parasitoid wasp Ascobara tabida and the red spider mite Tetranychus urticae experience both a reduction in survival and reproductive output as diapause duration increases (Kroon and Veenendaal 1998; Ellers and Van Alphen 2002). Similarly, in the Colorado potato beetle, Leptinotarsa decemlineata, females that experienced a two-year diapause are significantly less fecund and produce larvae with higher mortality rates than females that have been in diapause for only one year (Margus and Lindström 2020). But, interestingly, there are no differences in fecundity or larval survival of males that experienced a two vs. one year diapause, again illustrating sex-specific trade-offs between diapause and fitness that disproportionately impact female insects.

Male contributions allowing females to override trade-offs

Given that certain species of female insects sustain a fitness cost from having to survive the winter, males of these species might possess some compensatory mechanisms allowing females to overcome these reproductive trade-offs. Notably, males of several insect species provision females with a protein-rich spermatophore that not only protects the sperm but can also be used as a source of nutrition. In the Japanese common grass yellow butterfly, Eurema mandarina, diapausing females can mate with older, summer-morph males prior to entering diapause, but they also frequently mate with post-diapause males the following spring (Kato 1986). Mated diapausing females rapidly deplete their spermatophores, remate with post-diapause males early in the season, and survive longer than unmated females (Kato 1986; Konagaya and Watanabe 2015; Konagaya and Numata 2018), suggesting that diapausing female E. mandarina may mate with summer-morph males to exploit the spermatophore as an energy source.

In addition to providing spermatophores to females, males could also alter the composition and/or amount of ejaculate to facilitate immune priming or survival in diapausing females, or to promote higher fecundity in post-diapausing females. Changes in seminal fluid composition could be particularly pronounced in insect species where females mate before entering diapause and males die. In such cases, survival of the species is entirely dependent on females to not only successfully overwinter but to also maintain viable sperm. Alternatively, in cases where mating occurs after diapause termination, males could possibly alter their ejaculate to enhance the reproductive performance of post-diapause females, but this would require males to distinguish between post-diapausing and non-diapausing females. Ala-Honkola et al. (2020) demonstrated that males of D. montana can indeed discriminate between diapausing and post-diapausing females such that males do not attempt to court females until they have terminated diapause. Future studies are needed to determine whether males also deliver more sperm and/or a different suite of seminal fluid proteins to post-diapause and non-diapausing females in this and other insect species.

To date, the role of males in ameliorating reproductive trade-offs experienced by post-diapause females has not been extensively studied. In some preliminary experiments, we have measured the abundance of transcripts in the male accessory glands (the insect equivalent to mammalian prostate glands) in Northern house mosquitoes that were reared under summer-like or winter-like conditions. Our data demonstrate that male Cx. pipiens reared under long, summer days produce more transcripts associated with hormonal signaling and protein digestion in their accessory glands, and that non-diapausing females that mate with “summer” males are more likely to blood-feed and produce more offspring than those that mate with “winter” males (Meuti lab unpublished data). Additionally, we found that males reared in short-day, winter-like conditions produce more transcripts associated with immune functions and that diapausing females mated with “winter” males survive significantly longer than those mated with “summer” males (Meuti lab unpublished data). Similarly, Colgan et al. (2019) found that mating increases the abundance of antimicrobial peptides in the hemolymph of pre-diapausing queens of B. terrestris, and that these proteins remain elevated throughout the diapause program. Additional studies in diverse insect species will be useful for determining whether and how males alter their mating behavior and/or ejaculate composition to enhance survival and fecundity of pre- or post-diapausing females.

Impact of human-mediated changes to the environment on the trade-offs between diapause and reproduction

Both climate change and urbanization have the potential to profoundly impact the trade-offs between survival and reproduction experienced by diapausing female insects. Climate change not only is associated with an increase in overall temperatures, but also more variable winter conditions with repeated freeze-thaw cycles (Williams et al. 2015). As previously mentioned, overwintering female insects are particularly vulnerable to higher winter temperatures associated with climate change due to the increase in metabolic rate and hence the more rapid depletion of energetic reserves that may be necessary for subsequent reproduction (reviewed by Marshall et al. 2020; Tougeron et al. 2020). However, climate change can have varied and unanticipated impacts on insect fitness. For example, Sturiale and Armbruster (2023) demonstrated that winter heatwaves enhanced survival of diapausing embryos of Ae. albopictus. However, embryos that experienced a longer and warmer fall were less fit after terminating diapause, such that the resulting male and female larvae had lower resistance to starvation, higher mortality, and took longer to develop.

Additionally, climate change may present scenarios where insects enter a developmental trap by incorrectly interpreting seasonal cues and/or attempting to produce an additional generation at a time of year where it would be ecologically disastrous. Indeed, this has been demonstrated in populations of the wall brown butterfly, Lasiommata megera, in northwestern Europe (Van Dyck et al. 2015) and in populations of the mustard white butterfly, Pieris oleracea, in the northeastern United States (Kerr et al. 2020). However, as the climate continues to warm and the number of growing-degree days increases, it is likely that many species will successfully complete another generation within a growing season (Kerr et al. 2020). Additionally, climate change might drive some insect species to lose their capacity for diapause altogether, as suggested for certain aphid parasitoids in western France (Tougeron et al. 2017).

Urban habitats have higher levels of artificial light at night (ALAN) as well as higher temperatures relative to rural areas due to the UHI effect (reviewed by Deilami et al. 2018; Bará and Falchi 2023). Both light pollution and UHIs can influence fitness trade-offs that female insects experience (Mukai et al. 2021). For example, urban and rural populations of the tiger mosquito Ae. albopictus and geometrid moths, Chiasmia clathrata were equally likely to avert diapause upon exposure to low levels of ALAN (Westby and Medley 2020; Merckx et al. 2023). But there is also evidence that Nordic populations of P. napi and C. clathrata are adapting to urban environments by increasing the duration of their flight activity and postponing diapause initiation in response to higher temperatures associated with UHIs (Merckx et al. 2021). Additionally, winter-adapted urban and rural populations of the acorn ant, Temnothorax curvispinosus, show similar levels of chill coma recovery time and metabolic suppression in response to low temperatures, but winter-adapted ants from urban environments have a higher heat tolerance (Prileson et al. 2023). Taken together, these data suggest that some overwintering insects are able to adapt to higher temperatures in urban environments but may remain sensitive to light pollution.

Recent work from our laboratory also indicates that urbanization can impact the trade-offs associated with diapause and reproduction. For example, exposing Cx. pipiens to either low levels of light pollution or slightly higher temperatures that characterize the UHI effect in the laboratory causes female mosquitoes reared under short photoperiods to avert diapause (Fyie et al. 2021, 2023). However, female mosquitoes exposed to either ALAN or UHI temperatures have higher levels of fat than nondiapausing females, suggesting that light pollution and elevated temperatures may uncouple physiological pathways that regulate diapause and thereby remove trade-offs between current reproduction and later survival. Additionally, ALAN differentially affects seasonal activity levels in mosquitoes, such that exposure to light pollution increases the overall activity of short-day-reared females and decreases activity in long-day-reared females (Wolkoff et al. 2023). Most recently, we found that short-day-reared female mosquitoes that are continuously exposed to ALAN have lower survival rates than those that are reared in standard light-dark cycles (Fiorta unpublished data). Thus, taken together, our data suggest that light pollution and UHIs can alter seasonal differences in mosquito survival, behavior, and reproduction.

Conclusions and future directions

Females of many insect species face trade-offs between diapause entry and reproduction, and these trade-offs can occur whether the female overwinters as an egg, larva, pupa, or adult. However, there are also many examples where diapause does not appear to impact the fecundity of post-diapause females (Beekman et al. 1998; Wang et al. 2006; Musolin et al. 2007). These different fitness outcomes could be caused by differences in reproductive strategies, such that reproducing females that depend on nutrient reserves sequestered early in life (e.g., capital breeders) may face greater reproductive trade-offs than females that use nutrients they obtain later to produce offspring (e.g., income breeders; reviewed by Denlinger 2022). Indeed, differences in diapause timing based on differences in reproductive strategy have been elegantly modeled by Varpe and Ejsmond (2018).

Additionally, post-diapause female insects generally show greater fitness deficits than males (Denlinger 1981; Margus and Lindström 2020), although there are several examples in which both post-diapause males and females are less fertile than their non-diapausing counterparts (Sadakiyo and Ishihara 2012; Kubrak et al. 2016). These species-specific differences may not only represent differences in the energetic investment strategy for reproduction (e.g., capital vs. income breeding) but also when reproductive maturation occurs. For example, spermatogenesis occurs in the late larval stage or pupal stage for many insects. Therefore, it is not surprising that diverting resources away from reproductive development towards survival imposes fitness costs, as demonstrated in male codling moths, spotted stem borers, and bruchid beetles (Deseo 1973; Sadakiyo and Ishihara 2012; Dhillon and Hasan 2018). We are, however, not aware of cases where post-diapause males suffer reduced fitness and females do not, further emphasizing the higher energetic investment that both diapause and reproduction impose on females.

Though it has not been extensively studied, male insects may be able to alleviate reproductive trade-offs that post-diapause females experience. For example, in species where females overwinter in a mated state, males could provision females with spermatophores or other ejaculatory components that could help nourish and sustain them (Kato 1986; Konagaya and Watanabe 2015; Konagaya and Numata 2018). Alternatively, mating before the winter might impose an additional fitness cost for females, as they would have to invest some of their energetic reserves to maintain and store sperm. Future studies are needed to quantify the amount of energy that mated, diapausing female insects invest in sperm maintenance. In species that overwinter as immature stages, or that overwinter as unmated adult males and females, it will be interesting to examine whether males alter the composition or amount of their ejaculate in response to the diapause status of the female to enable her to produce a high number of offspring.

Measuring both the timing and duration of diapause and the post-diapause reproductive potential of females makes it possible to produce accurate models of population growth, range expansion, and voltinism in arthropods (Taylor 1986; Musolin and Numata 2003; Jönsson et al. 2011; Montero-Pau et al. 2014; Mushegian et al. 2021). Additionally, given the marked changes in temperature and light cues caused by climate change and urbanization, it is becoming imperative for us to better characterize how female insects manage their energetic budget to not only survive increasingly warm and variable winter conditions but to then also subsequently reproduce. The current literature demonstrates that impacts of human-mediated changes to the environment are complex and difficult to predict. For example, climate change and urbanization can enhance some fitness traits and decrease others, both within populations (Fyie et al. 2021, 2023; Sturiale and Armbruster 2023) and across different populations (Kerr et al. 2020; Merckx et al. 2021). Possibly some insect species will minimize trade-offs between overwintering survival and reproduction, and thereby not only survive but thrive in our warming and increasingly urbanized world. In contrast, climate change and/or urbanization may exacerbate trade-offs in other species, possibly leading to local or total extinction. It is thus critical to employ both field and laboratory studies to determine how trade-offs between winter survival and reproduction are impacting diverse insect species in the Anthropocene.

Notes

From the symposium “What do trade-offs mean to reproducing females?: An integrative look at whole-organism trade-offs” presented at the in--person annual meeting of the Society for Integrative and Comparative Biology, January 16–March 31, 2024.

Funding

This work was supported by the National Science Foundation [Grant number IOS-1,944,323] awarded to M.M., the United States Department of Agriculture [Grant number 2023-67,013-39,915] awarded to M.M., and by state and federal funds appropriated to The Ohio State University, College of Food, Agricultural, and Environmental Sciences to M.M. and L.F. This project was further supported by the USDA National Institute of Food and Agriculture, Hatch Multi-State project NE 1943.

Conflict of interest

We declare no conflict of interests.

Data Availability

The data underlying this article are available in the article.