Fitness under high temperatures is overestimated when daily thermal fluctuation is ignored.

Experimental studies on the thermal biology of organisms have become crucial to investigate the impact of climate warming. However, most laboratory studies are carried out under constant temperatures and assume a negligible effect from daily fluctuating temperatures. We tested this assumption on multiple fitness traits of the moth Spodoptera littoralis, and a literature review on insects complements this study. Tests on S. littoralis focused on its optimal and maximal critical temperatures by comparing constant and daily fluctuating temperatures (±5 °C) at mean temperatures of 25, 29 and 33 °C. The nine fitness parameters investigated were influenced by mean temperature. The overall effect was a maximal multiplication rate at 29 °C and a marked decrease under the fluctuating regime at 33 °C. Effects of fluctuating temperatures differed between mean temperatures. Developmental and larval survival rates at 33 °C were lower under the fluctuating thermal regime than under a constant temperature. Our literature review also illustrates that ignoring daily fluctuations based on constant temperatures commonly leads to overestimate fitness traits at high temperatures. Overlooking the experimental bias associated with constant temperatures minimizes the expected impact of climate warming on fitness traits.

Effects of DEHP on the ecdysteroid pathway, sexual behavior and offspring of the moth Spodoptera littoralis.

Bis(2-ethylhexyl) phthalate (DEHP) is a widely produced plasticizer that is considered to act as an endocrine-disrupting chemical in vertebrates and invertebrates. Indeed, many studies have shown that DEHP alters hormonal levels, reproduction and behavior in vertebrates. Few studies have focused on the effects of DEHP on insects, although DEHP is found almost everywhere in their natural habitats, particularly in soils and plants. Here, we investigated the effects of DEHP on the sexual behavior and physiology of a pest insect, the noctuid moth Spodoptera littoralis. In this nocturnal species, olfaction is crucial for sexual behavior, and ecdysteroids at the antennal level have been shown to modulate sex pheromone detection by males. In the present study, larvae were fed food containing different DEHP concentrations, and DEHP concentrations were then measured in the adults (males and females). Hemolymphatic ecdysteroid concentrations, the antennal expression of genes involved in the ecdysteroid pathway (nuclear receptors EcR, USP, E75, and E78 and calmodulin) and sexual behavior were then investigated in adult males. The success and latency of mating as well as the hatching success were also studied in pairs consisting of one DEHP male and one uncontaminated female or one DEHP female and one uncontaminated male. We also studied the offspring produced from pairs involving contaminated females to test the transgenerational effect of DEHP. Our results showed the general downregulation of nuclear receptors and calmodulin gene expression associated with the higher concentrations of DEHP, suggesting peripheral olfactory disruption. We found some effects on male behavior but without an alteration of the mating rate. Effects on offspring mortality and developmental rates in the N + 1 generation were also found at the higher doses of DEHP. Taken together, the results of the study show for the first time that larval exposure to DEHP can induce delayed endocrine-disruptive effects in the adults of a terrestrial insect as well as effects on the next generation. To date, our study is also the first description of an impact of endocrine disrupter on olfaction in insects.

A maternal effect influences sensitivity to chlorpyrifos pesticide in the pest moth Spodoptera littoralis.

Transgenerational effects on sensitivity to pesticides are poorly studied. This study investigated the transgenerational influences of maternal body mass in the major pest moth Spodoptera littoralis, with a focus on sensitivity to chlorpyrifos pesticide. In 147 clutches of a laboratory strain of S. littoralis, we compared larval mortality between control larvae and larvae treated with chlorpyrifos. Because of the classic positive relationships between offspring size and maternal size and between offspring size and offspring quality, sensitivity to chlorpyrifos was predicted to be lower in larvae of larger mothers. Surprisingly, we found the opposite result, with higher pesticide toxicity in larvae of larger mothers. This result is partly explained by the lack of a relationship between larval mass and larval sensitivity to chlorpyrifos. This means that another offspring characteristic linked to maternal size should have affected larval sensitivity to chlorpyrifos. More generally, knowledge of the effects of the traits and ecological environments of mothers on offspring sensitivity to pesticides remains limited. Ecotoxicologists should pay more attention to such maternal effects on sensitivity to pesticides, both in pests and non-target species.

The sex chromosome system can influence the evolution of sex-biased dispersal.

Sex-biased dispersal is a much-discussed feature in literature on dispersal. Diverse hypotheses have been proposed to explain the evolution of sex-biased dispersal, a difference in dispersal rate or dispersal distance between males and females. An early hypothesis has indicated that it may rely on the difference in sex chromosomes between males and females. However, this proposal was quickly rejected without a real assessment. We propose a new perspective on this hypothesis by investigating the evolution of sex-biased dispersal when dispersal genes are sex-linked, that is when they are located on the sex chromosomes. We show that individuals of the heterogametic sex disperse relatively more than do individuals of the homogametic sex when dispersal genes are sex-linked rather than autosomal. Although such a sex-biased dispersal towards the heterogametic sex is always observed in monogamous species, the mating system and the location of dispersal genes interact to modulate sex-biased dispersal in monandry and polyandry. In the context of the multicausality of dispersal, we suggest that sex-linked dispersal genes can influence the evolution of sex-biased dispersal.

Climate warming: a loss of variation in populations can accompany reproductive shifts.

The most documented response of organisms to climate warming is a change in the average timing of seasonal activities (phenology). Although we know that these average changes can differ among species and populations, we do not know whether climate warming impacts within-population variation in phenology. Using data from five study sites collected during a 13-year survey, we found that the increase in spring temperatures is associated with a reproductive advance of 10 days in natural populations of common lizards (Zootoca vivipara). Interestingly, we show a correlated loss of variation in reproductive dates within populations. As illustrated by a model, this shortening of the reproductive period can have significant negative effects on population dynamics. Consequently, we encourage tests in other species to assess the generality of decreased variation in phenological responses to climate change.

Dispersal as a source of variation in age-specific reproductive strategies in a wild population of lizards.

Dispersal syndromes describe the patterns of covariation of morphological, behavioural, and life-history traits associated with dispersal. Studying dispersal syndromes is critical to understanding the demographic and genetic consequences of movements. Among studies describing the association of life-history traits with dispersal, there is anecdotal evidence suggesting that dispersal syndromes can vary with age. Recent theory also suggests that dispersive and philopatric individuals might have different age-specific reproductive efforts. In a wild population of the common lizard (Zootoca vivipara), we investigated whether dispersive and philopatric individuals have different age-specific reproductive effort, survival, offspring body condition, and offspring sex ratio. Consistent with theoretical predictions, we found that young dispersive females have a higher reproductive effort than young philopatric females. Our results also suggest that the early high investment in reproduction of dispersive females trades-off with an earlier onset of senescence than in philopatric females. We further found that young dispersive females produce smaller offspring in lower body condition than do young philopatric females. Overall, our results provide empirical evidence that dispersive and philopatric individuals have different age-specific life-history traits.

The effect of developmental temperature on olfaction in a moth revealed by its interaction with body mass.

There is a growing interest in the effects of climate warming on olfaction, as temperature may affect this essential sense. In insects, the response of the olfactory system to developmental temperature might be mediated by body size or mass because body size and mass are negatively affected by developmental temperature in most ectotherms. We tested this hypothesis of a mass-mediated effect of developmental temperature on olfaction in the moth Spodoptera littoralis. We measured the olfactory sensitivity of male to female sex pheromone and five plant odors using electroantennography. We compared males reared at an optimal temperature (25 °C with a daily fluctuation of ±5 °C) and at a high temperature (33 ± 5 °C) close to the upper limit of S. littoralis. On average, the olfactory sensitivity of males did not differ between the two developmental temperatures. However, our analyses revealed an interaction between the effects of developmental temperature and body mass on the detection of the six chemicals tested. This interaction is explained by a positive relationship between antennal sensitivity and body mass observed only with the high developmental temperature. Our results show that the effect of developmental temperature may not be detected when organism size is ignored.

Daily temperature fluctuation interacts with the mean temperature to increase the toxicity of a pyrethroid insecticide in a moth.

Climate change complicates ecotoxicology studies because species responses to pesticides depend on temperature. Classically illustrated by the effect of constant laboratory temperatures, a recent review revealed that the toxicity of pesticides is also often increased by daily temperature fluctuations. Here, we investigated the combined effects of daily temperature fluctuation and mean temperature on the toxicity of two insecticides in the moth Spodoptera littoralis. Our study tested the toxicity of chlorpyrifos and deltamethrin on larvae of six experimental groups that crossed three treatments of daily temperature fluctuations (0, 5 or 10 °C) and two treatments of mean temperatures (25 or 33 °C). We showed that daily temperature fluctuation increased larval mortality induced by chlorpyrifos and deltamethrin. However, the response differed between the organophosphorus insecticide chlorpyrifos and the pyrethroid insecticide deltamethrin. The increase in chlorpyrifos toxicity by daily temperature fluctuation did not differ between mean temperatures of 25 and 33 °C. Remarkably, the increase in deltamethrin toxicity by daily temperature fluctuation was dependent on the crossed effects of the amplitude of daily fluctuation and mean temperature. This increase in deltamethrin toxicity occurred with a daily fluctuation of only 5 °C for larvae reared at 25 °C and a daily fluctuation of 10 °C in larvae reared at 33 °C. To confidently quantify the responses of insecticide toxicity to temperature, future ecotoxicology studies will have to evaluate the generality of the interaction between the effects of daily temperature fluctuation and mean temperature.

Reproductive allocation strategies: a long-term study on proximate factors and temporal adjustments in a viviparous lizard.

Optimisation of reproductive investment is crucial for Darwinian fitness, and detailed long-term studies are especially suited to unravel reproductive allocation strategies. Allocation strategies depend on the timing of resource acquisition, the timing of resource allocation, and trade-offs between different life-history traits. A distinction can be made between capital breeders that fuel reproduction with stored resources and income breeders that use recently acquired resources. In capital breeders, but not in income breeders, energy allocation may be decoupled from energy acquisition. Here, we tested the influence of extrinsic (weather conditions) and intrinsic (female characteristics) factors during energy storage, vitellogenesis and early gestation on reproductive investment, including litter mass, litter size, offspring mass and the litter size and offspring mass trade-off. We used data from a long-term study of the viviparous lizard, Lacerta (Zootoca) vivipara. In terms of extrinsic factors, rainfall during vitellogenesis was positively correlated with litter size and mass, but temperature did not affect reproductive investment. With respect to intrinsic factors, litter size and mass were positively correlated with current body size and postpartum body condition of the previous year, but negatively with parturition date of the previous year. Offspring mass was negatively correlated with litter size, and the strength of this trade-off decreased with the degree of individual variation in resource acquisition, which confirms theoretical predictions. The combined effects of past intrinsic factors and current weather conditions suggest that common lizards combine both recently acquired and stored resources to fuel reproduction. The effect of past energy store points out a trade-off between current and future reproduction.

Experimental litter size reduction reveals costs of gestation and delayed effects on offspring in a viviparous lizard.

Experimental studies have often been employed to study costs of reproduction, but rarely to study costs of gestation. Disentangling the relative importance of each stage of the reproductive cycle should help to assess the costs and benefits of different reproductive strategies. To that end, we experimentally reduced litter size during gestation in a viviparous lizard. We measured physiological and behavioural parameters during gestation and shortly after parturition, as well as survival and growth of females and their offspring. This study showed four major results. First, the experimental litter size reduction did not significantly affect the cellular immune response, the metabolism and the survival of adult females. Second, females with reduced litter size decreased their basking time. Third, these females also had an increased postpartum body condition. As postpartum body condition is positively related to future reproduction, this result indicates a gestation cost. Fourth, even though offspring from experimentally reduced litters had similar weight and size at birth as other offspring, their growth rate after birth was significantly increased. This shows the existence of a maternal effect during gestation with delayed consequences. This experimental study demonstrates that there are some costs to gestation, but it also suggests that some classical trade-offs associated with reproduction may not be explained by gestation costs.

Litter quality and inflammatory response are dependent on mating strategy in a reptile.

Maintenance of health and the production of offspring are competing processes that can result in trade-offs. As vertebrates invest substantial resources in their immune system, it is crucial to understand the interactions between immunity and reproductive strategies. In the lizard Zootoca vivipara, females have condition- and context-dependent mating strategies. We predicted that, if the risk of infection is higher for polyandrous females, then polyandrous females should invest more in immune system while monandrous females should invest more in reproduction. In order to test our prediction, we captured 62 gravid females of known age in a natural population; we kept them until parturition to access to their offspring. Then, using microsatellite marker-based paternity analyses within litters, we determine the mating strategy of females (monandrous or polyandrous). Females were also challenged with PHA to estimate their inflammatory response. Our results show that polyandrous females have a higher PHA response than the monandrous females, and that monandrous females produce more males and more juveniles of better body condition than polyandrous females. The relationship between mating behaviour and immune function may have consequences for females and may shape the evolution of mating systems.

The impact of temperature on insecticide sensitivity depends on transgenerational effects.

The combined effects of insecticides and temperature are increasingly being studied because species are expected to change their responses to insecticides with climate warming. As recently highlighted, the impact of temperature on insecticide sensitivity might be influenced by the environment experienced by the previous generation. However, a pioneering study that showed this transgenerational effect in the mosquito Culex pipiens needs to be confirmed because two other studies did not show similar results. Here, we performed an experiment on the moth Spodoptera littoralis to test this hypothesis. We analysed reaction norms among experimental families to test transgenerational effects, i.e., the variation in the response of families to the combined effects of the insecticide chlorpyrifos and developmental temperature. Reaction norm analyses revealed that the responses of the families to chlorpyrifos and temperature differed for developmental time and larval survival, two key parameters in S. littoralis. Crucially, for larval survival, a family effect influenced the impact of temperature on chlorpyrifos sensitivity. This finding confirms the pioneering study on C. pipiens that showed transgenerational effects on the combined effects of insecticides and temperature. This result also highlights that transgenerational plasticity can be important to consider in ecotoxicology.

Combined influences of transgenerational effects, temperature and insecticide on the moth Spodoptera littoralis.

Climate warming is expected to impact the response of species to insecticides. Recent studies show that this interaction between insecticides and temperature can depend on other factors. Here, we tested for the influence of transgenerational effects on the Insecticide × Temperature interaction in the crop pest moth Spodoptera littoralis. Specifically, we analysed reaction norms among experimental clutches based on a split-plot design crossing the factors temperature, insecticide and clutch. The study was performed on 2280 larvae reared at four temperatures (23, 25, 27 and 29 °C), and their response to the insecticide deltamethrin (three concentrations and a control group) was tested. Temperature had a global influence with effects on larval survival, duration of development, pupal body mass, and significant reaction norms of the clutches for temperature variations of only 2 °C. In addition to the expected effect of deltamethrin on mortality, the insecticide slightly delayed the development of S. littoralis, and the effects on mortality and development differed among the clutches. Projection models integrating all the observed responses illustrated the additive effects of deltamethrin and temperature on the population multiplication rate. Variation in the response of the clutches showed that transgenerational effects influenced the impact of insecticide and temperature. Although no evidence indicated that the Insecticide × Temperature interaction depended on transgenerational effects, the studies on the dependence of the Insecticide × Temperature interaction on other factors continue to be crucial to confidently predict the combined effects of insecticides and climate warming.

Cohort variation, climate effects and population dynamics in a short-lived lizard.

1. Demographic theory and empirical studies indicate that cohort variation in demographic traits has substantial effects on population dynamics of long-lived vertebrates but cohort effects have been poorly investigated in short-lived species. 2. Cohort effects were quantified in the common lizard (Zootoca vivipara Jacquin 1787), a short-lived ectothermic vertebrate, for body size, reproductive traits and age-specific survival with mark-recapture data collected from 1989 to 2005 in two wetlands. We assessed cohort variation and covariation in demographic traits, tested the immediate and delayed effects of climate conditions (temperature and rainfall), and predicted consequences for population growth. 3. Most demographic traits exhibited cohort variation, but this variation was stronger for juvenile growth and survival, sub-adult survival and breeding phenology than for other traits. 4. Cohort variation was partly explained by a web of immediate and delayed effects of climate conditions. Rainfall and temperature influenced distinct life-history traits and the periods of gestation and early juvenile life were critical stages for climate effects. 5. Cohort covariation between demographic traits was usually weak, apart from a negative correlation between juvenile and sub-adult body growth suggesting compensatory responses. An age-structured population model shows that cohort variation influences population growth mainly through direct numerical effects of survival variation early in life. 6. An understanding of cohort effects is necessary to predict critical life stages and climatic determinants of population dynamics, and therefore demographic responses to future climate warming.

Effects of low concentrations of deltamethrin are dependent on developmental stages and sexes in the pest moth Spodoptera littoralis.

Effects of low concentrations of pesticides, with no or moderate mortality of targeted species, are poorly studied even though these low concentrations are common under natural conditions. Studying their effects is critical because they can induce positive hormetic responses, possibly leading to greater pest multiplication and promoting the evolution of pest resistance. Here, we investigated the responses of the pest moth Spodoptera littoralis to low concentrations of deltamethrin, and tested for variation in effects of the pesticide between developmental stages and sexes. Indeed, we show that a given concentration of deltamethrin has different effects between stages, and even between sexes. Two experimental concentrations led to very high mortality early in S. littoralis development (4th larval instar), but only to low mortality rates in adults. Moreover, our highest experimental concentration had only detrimental effects in adult females, but improved the reproductive success of adult males. Model projections showed that the lethality from treatments at the 4th larval instar was the predominant effect. Because of the high multiplication rate of S. littoralis, it was also found that treatments with very similar effects on larval mortality can lead to either population extinction or rapid pest resurgence.

Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations.

There is accumulating evidence that individuals leave their natal area and select a breeding habitat non-randomly by relying upon information about their natal and future breeding environments. This variation in dispersal is not only based on external information (condition dependence) but also depends upon the internal state of individuals (phenotype dependence). As a consequence, not all dispersers are of the same quality or search for the same habitats. In addition, the individual's state is characterized by morphological, physiological or behavioural attributes that might themselves serve as a cue altering the habitat choice of conspecifics. These combined effects of internal and external information have the potential to generate complex movement patterns and could influence population dynamics and colonization processes. Here, we highlight three particular processes that link condition-dependent dispersal, phenotype-dependent dispersal and habitat choice strategies: (1) the relationship between the cause of departure and the dispersers' phenotype; (2) the relationship between the cause of departure and the settlement behaviour and (3) the concept of informed dispersal, where individuals gather and transfer information before and during their movements through the landscape. We review the empirical evidence for these processes with a special emphasis on vertebrate and arthropod model systems, and present case studies that have quantified the impacts of these processes on spatially structured population dynamics. We also discuss recent literature providing strong evidence that individual variation in dispersal has an important impact on both reinforcement and colonization success and therefore must be taken into account when predicting ecological responses to global warming and habitat fragmentation.

Relationship between female mating strategy, litter success and offspring dispersal.

The relationship between mating systems and dispersal has generally been studied at the population and species levels. It has hardly ever been investigated at the individual level, by studying the variations of mating and dispersal strategies between individuals. We investigated this relationship in a natural population of the common lizard (Lacerta vivipara). Assuming that dispersal has a genetic basis, juvenile dispersal would be expected to be more family-dependent in monoandrous litters than in polyandrous litters. The opposite pattern was observed. Thus, maternal effects and/or litter effects play a greater role than genetic determinism in shaping the dispersal phenotype of juveniles. Moreover, the relationship between female mating strategy and offspring dispersal depended on litter success, in a way consistent with an influence of mother-offspring competition. Such a link between mating and dispersal strategies of individuals may have major repercussions for the way we consider the roles of these processes in population functioning.

Intergenerational effects of climate generate cohort variation in lizard reproductive performance.

An evaluation of the link between climate and population dynamics requires understanding of climate effects both within and across generations. In ectothermic vertebrates, demographic responses to climate changes should crucially depend on balancing needs for heat and water. Here, we studied how temperature and rainfall regimes experienced before and during adulthood influenced reproductive performances (litter size, offspring size, and survival) in a natural population of the live-bearing common lizard, Lacerta vivipara, monitored continuously from 1989 to 2004. Rainfall regime, but not temperature, had both immediate and delayed effects on these reproductive performances. Rainfall during the first month of life was positively correlated with juvenile survival. Females experiencing more rainfall during gestation produced smaller neonates that showed greater survival when controlling for the positive effect of body size on survival. Furthermore, females that experienced heavier rainfall when in utero produced fewer but longer neonates during adulthood. These demographic effects of rainfall on adult reproductive traits may come from maternal effects of climate conditions and/or from delayed effects of rainfall on the environment experienced early in life. Irrespective of the precise mechanism, however, this study provides evidence of intergenerational climate effects in natural populations of an ectothermic vertebrate.

Condition dependence of reproductive strategy and the benefits of polyandry in a viviparous lizard.

Species in which males do not contribute to reproduction beyond the provision of sperm offer good opportunities to study the potential genetic benefits that females can obtain from polyandry. Here, we report the results of a study examining the relationships between polyandry and components of female fitness in the common lizard (Lacerta vivipara). We found that polyandrous females produce larger clutches than monandrous females. Polyandrous females also lose fewer offspring during the later stages of gestation and at birth, but we did not find any relationship between polyandry and physical characteristics of viable neonates. Our results were consistent with the predictions of the intrinsic male quality hypothesis, while inbreeding avoidance and genetic incompatibility avoidance might also explain some part of the variation observed in clutch size. Moreover, the benefits of polyandry appeared to depend on female characteristics, as revealed by an interaction between reproductive strategy and female length on reproductive success. Thus, all females did not benefit equally from mating with multiple males, which could explain why polyandry and monandry coexist.

Long-lasting fitness consequences of prenatal sex ratio in a viviparous lizard.

Maternal effects and early environmental conditions are important in shaping offspring developmental trajectories. For example, in laboratory mammals, the sex ratio during gestation has been shown to influence fitness-related traits via hormonal interaction between fetuses. Such effects have the potential to shape, or constrain, many important aspects of the organism's life, but their generality and importance in natural populations remain unknown. Using long-term data in a viviparous lizard, Lacerta vivipara, we investigated the relationship between prenatal sex ratio and offspring growth, survival, and reproductive traits as adults. Our results show that females from male-biased clutches grow faster, mature earlier, but have lower fecundity than females from female-biased clutches. Furthermore, male reproduction was also affected by the sex ratio during embryonic development, with males from male-biased clutches being more likely to successfully reproduce at age one than males from female-biased clutches. Thus, the sex ratio experienced during gestation can have profound and long-lasting effects on fitness in natural populations of viviparous animals, with important implications for life-history evolution and sex allocation.