Heatwaves are detrimental to fertility in the viviparous tsetse fly.

Heatwaves are increasing in frequency and intensity due to climate change, pushing animals beyond physiological limits. While most studies focus on survival limits, sublethal effects on fertility tend to occur below lethal thresholds, and consequently can be as important for population viability. Typically, male fertility is more heat-sensitive than female fertility, yet direct comparisons are limited. Here, we measured the effect of experimental heatwaves on tsetse flies, Glossina pallidipes, disease vectors and unusual live-bearing insects of sub-Saharan Africa. We exposed males or females to a 3-day heatwave peaking at 36, 38 or 40°C for 2 h, and a 25°C control, monitoring mortality and reproduction over six weeks. For a heatwave peaking at 40°C, mortality was 100%, while a 38°C peak resulted in only 8% acute mortality. Females exposed to the 38°C heatwave experienced a one-week delay in producing offspring, whereas no such delay occurred in males. Over six weeks, heatwaves resulted in equivalent fertility loss in both sexes. Combined with mortality, this lead to a 10% population decline over six weeks compared to the control. Furthermore, parental heatwave exposure gave rise to a female-biased offspring sex ratio. Ultimately, thermal limits of both survival and fertility should be considered when assessing climate change vulnerability.

Systematic approaches to assessing high-temperature limits to fertility in animals.

Critical thermal limits (CTLs) gauge the physiological impact of temperature on survival or critical biological function, aiding predictions of species range shifts and climatic resilience. Two recent Drosophila species studies, using similar approaches to determine temperatures that induce sterility (thermal fertility limits [TFLs]), reveal that TFLs are often lower than CTLs and that TFLs better predict both current species distributions and extinction probability. Moreover, many studies show fertility is more sensitive at less extreme temperatures than survival (thermal sensitivity of fertility [TSF]). These results present a more pessimistic outlook on the consequences of climate change. However, unlike CTLs, TFL data are limited to Drosophila, and variability in TSF methods poses challenges in predicting species responses to increasing temperature. To address these data and methodological gaps, we propose 3 standardized approaches for assessing thermal impacts on fertility. We focus on adult obligate sexual terrestrial invertebrates but also provide modifications for other animal groups and life-history stages. We first outline a "gold-standard" protocol for determining TFLs, focussing on the effects of short-term heat shocks and simulating more frequent extreme heat events predicted by climate models. As this approach may be difficult to apply to some organisms, we then provide a standardized TSF protocol. Finally, we provide a framework to quantify fertility loss in response to extreme heat events in nature, given the limitations in laboratory approaches. Applying these standardized approaches across many taxa, similar to CTLs, will allow robust tests of the impact of fertility loss on species responses to increasing temperatures.

A theoretical model for host-controlled regulation of symbiont density.

There is growing empirical evidence that animal hosts actively control the density of their mutualistic symbionts according to their requirements. Such active regulation can be facilitated by compartmentalization of symbionts within host tissues, which confers a high degree of control of the symbiosis to the host. Here, we build a general theoretical framework to predict the underlying ecological drivers and evolutionary consequences of host-controlled endosymbiont density regulation for a mutually obligate association between a host and a compartmentalized, vertically transmitted symbiont. Building on the assumption that the costs and benefits of hosting a symbiont population increase with symbiont density, we use state-dependent dynamic programming to determine an optimal strategy for the host, i.e., that which maximizes host fitness, when regulating the density of symbionts. Simulations of active host-controlled regulation governed by the optimal strategy predict that the density of the symbiont should converge to a constant level during host development, and following perturbation. However, a similar trend also emerges from alternative strategies of symbiont regulation. The strategy which maximizes host fitness also promotes symbiont fitness compared to alternative strategies, suggesting that active host-controlled regulation of symbiont density could be adaptive for the symbiont as well as the host. Adaptation of the framework allowed the dynamics of symbiont density to be predicted for other host-symbiont ecologies, such as for non-essential symbionts, demonstrating the versatility of this modelling approach.

Stress in the social context: a behavioural and eco-evolutionary perspective.

The social environment is one of the primary sources of challenging stimuli that can induce a stress response in animals. It comprises both short-term and stable interactions among conspecifics (including unrelated individuals, mates, potential mates and kin). Social stress is of unique interest in the field of stress research because (1) the social domain is arguably the most complex and fluctuating component of an animal's environment; (2) stress is socially transmissible; and (3) stress can be buffered by social partners. Thus, social interactions can be both the cause and cure of stress. Here, we review the history of social stress research, and discuss social stressors and their effects on organisms across early life and adulthood. We also consider cross-generational effects. We discuss the physiological mechanisms underpinning social stressors and stress responses, as well as the potential adaptive value of responses to social stressors. Finally, we identify outstanding challenges in social stress research, and propose a framework for addressing these in future work.

The complex interactions between nutrition, immunity and infection in insects.

Insects are the most diverse animal group on the planet. Their success is reflected by the diversity of habitats in which they live. However, these habitats have undergone great changes in recent decades; understanding how these changes affect insect health and fitness is an important challenge for insect conservation. In this Review, we focus on the research that links the nutritional environment with infection and immune status in insects. We first discuss the research from the field of nutritional immunology, and we then investigate how factors such as intracellular and extracellular symbionts, sociality and transgenerational effects may interact with the connection between nutrition and immunity. We show that the interactions between nutrition and resistance can be highly specific to insect species and/or infection type - this is almost certainly due to the diversity of insect social interactions and life cycles, and the varied environments in which insects live. Hence, these connections cannot be easily generalised across insects. We finally suggest that other environmental aspects - such as the use of agrochemicals and climatic factors - might also influence the interaction between nutrition and resistance, and highlight how research on these is essential.

How plastic are upper thermal limits? A comparative study in tsetse (family: Glossinidae) and wider Diptera.

Critical thermal maximum (CTmax) describes the upper thermal tolerance of an animal where biological functions start to fail. A period of acclimation can enhance CTmax through plasticity, potentially buffering animals from extreme temperatures caused by climate change. Basal and acclimated CTmax vary within and between species and may be explained by traits related to thermal physiology, such as body size and sex. Differences in CTmax have not been established among species of tsetse fly (Glossina spp.), vectors of animal and human African trypanosomiasis. Here, we investigated basal CTmax and its plasticity for five tsetse species following adult acclimation at constant 25 or 30 °C for five days. We then set our findings in context using a meta-analysis on 33 species of Diptera. We find that, of the five tsetse species considered, only Glossina palpalis gambiensis and Glossina brevipalpis exhibited plasticity of CTmax, with an increase of 0.12 °C and 0.10 °C per 1 °C acclimation respectively. Within some species, higher basal CTmax values were associated with larger body size and being female, while variation in plasticity (i.e., response to the acclimation temperature) could not be explained by sex or size. Our broader meta-analysis across Diptera revealed overall CTmax plasticity of 0.06 °C per 1 °C acclimation, versus a similar 0.05 °C mean increase in tsetse. In contrast, there was greater CTmax plasticity in males compared to females in Diptera. Our study highlights that CTmax and its plasticity varies even among closely related species. Broader patterns across groups are not always reflected at a finer resolution; we thus emphasise the need for detailed experimental studies across a wide range of insect species to capture their capacity to cope with rapidly warming temperatures.

Incorporating effects of age on energy dynamics predicts nonlinear maternal allocation patterns in iteroparous animals.

Iteroparous parents face a trade-off between allocating current resources to reproduction versus maximizing survival to produce further offspring. Parental allocation varies across age and follows a hump-shaped pattern across diverse taxa, including mammals, birds and invertebrates. This nonlinear allocation pattern lacks a general theoretical explanation, potentially because most studies focus on offspring number rather than quality and do not incorporate uncertainty or age-dependence in energy intake or costs. Here, we develop a life-history model of maternal allocation in iteroparous animals. We identify the optimal allocation strategy in response to stochasticity when energetic costs, feeding success, energy intake and environmentally driven mortality risk are age-dependent. As a case study, we use tsetse, a viviparous insect that produces one offspring per reproductive attempt and relies on an uncertain food supply of vertebrate blood. Diverse scenarios generate a hump-shaped allocation when energetic costs and energy intake increase with age and also when energy intake decreases and energetic costs increase or decrease. Feeding success and environmentally driven mortality risk have little influence on age-dependence in allocation. We conclude that ubiquitous evidence for age-dependence in these influential traits can explain the prevalence of nonlinear maternal allocation across diverse taxonomic groups.

An evolutionary perspective on stress responses, damage and repair.

Variation in stress responses has been investigated in relation to environmental factors, species ecology, life history and fitness. Moreover, mechanistic studies have unravelled molecular mechanisms of how acute and chronic stress responses cause physiological impacts ('damage'), and how this damage can be repaired. However, it is not yet understood how the fitness effects of damage and repair influence stress response evolution. Here we study the evolution of hormone levels as a function of stressor occurrence, damage and the efficiency of repair. We hypothesise that the evolution of stress responses depends on the fitness consequences of damage and the ability to repair that damage. To obtain some general insights, we model a simplified scenario in which an organism repeatedly encounters a stressor with a certain frequency and predictability (temporal autocorrelation). The organism can defend itself by mounting a stress response (elevated hormone level), but this causes damage that takes time to repair. We identify optimal strategies in this scenario and then investigate how those strategies respond to acute and chronic exposures to the stressor. We find that for higher repair rates, baseline and peak hormone levels are higher. This typically means that the organism experiences higher levels of damage, which it can afford because that damage is repaired more quickly, but for very high repair rates the damage does not build up. With increasing predictability of the stressor, stress responses are sustained for longer, because the animal expects the stressor to persist, and thus damage builds up. This can result in very high (and potentially fatal) levels of damage when organisms are exposed to chronic stressors to which they are not evolutionarily adapted. Overall, our results highlight that at least three factors need to be considered jointly to advance our understanding of how stress physiology has evolved: (i) temporal dynamics of stressor occurrence; (ii) relative mortality risk imposed by the stressor itself versus damage caused by the stress response; and (iii) the efficiency of repair mechanisms.

Competitive growth in a cooperative mammal.

In many animal societies where hierarchies govern access to reproduction, the social rank of individuals is related to their age and weight and slow-growing animals may lose their place in breeding queues to younger 'challengers' that grow faster. The threat of being displaced might be expected to favour the evolution of competitive growth strategies, where individuals increase their own rate of growth in response to increases in the growth of potential rivals. Although growth rates have been shown to vary in relation to changes in the social environment in several vertebrates including fish and mammals, it is not yet known whether individuals increase their growth rates in response to increases in the growth of particular reproductive rivals. Here we show that, in wild Kalahari meerkats (Suricata suricatta), subordinates of both sexes respond to experimentally induced increases in the growth of same-sex rivals by raising their own growth rate and food intake. In addition, when individuals acquire dominant status, they show a secondary period of accelerated growth whose magnitude increases if the difference between their own weight and that of the heaviest subordinate of the same sex in their group is small. Our results show that individuals adjust their growth to the size of their closest competitor and raise the possibility that similar plastic responses to the risk of competition may occur in other social mammals, including domestic animals and primates.

Big Baby, Little Mother: Tsetse Flies Are Exceptions to the Juvenile Small Size Principle.

While across the animal kingdom offspring are born smaller than their parents, notable exceptions exist. Several dipteran species belonging to the Hippoboscoidea superfamily can produce offspring larger than themselves. In this essay, the blood-feeding tsetse is focused on. It is suggested that the extreme reproductive strategy of this fly is enabled by feeding solely on highly nutritious blood, and producing larval offspring that are soft and malleable. This immense reproductive expenditure may have evolved to avoid competition with other biting flies. Tsetse also transmit blood-borne parasites that cause the fatal diseases called African trypanosomiases. It is discussed how tsetse life history and reproductive strategy profoundly influence the type of vector control interventions used to reduce fly populations. In closing, it is argued that the unusual life history of tsetse warrants their preservation in the areas where human and animal health is not threatened.

Effects of maternal age and stress on offspring quality in a viviparous fly.

Many organisms show signs of deterioration with age in terms of survival and reproduction. We tested whether intraspecific variation in such senescence patterns can be driven by resource availability or reproductive history. We did this by manipulating nutritional stress and age at first reproduction and measuring age-dependent reproductive output in tsetse (Glossina morsitans morsitans), a viviparous fly with high maternal allocation. Across all treatments, offspring weight followed a bell-shaped curve with maternal age. Nutritionally stressed females had a higher probability of abortion and produced offspring with lower starvation tolerance. There was no evidence of an increased rate of reproductive senescence in nutritionally stressed females, or a reduced rate due to delayed mating, as measured by patterns of abortion, offspring weight or offspring starvation tolerance. Therefore, although we found evidence of reproductive senescence in tsetse, our results did not indicate that resource allocation trade-offs or costs of reproduction increase the rate of senescence.

Insect-host control of obligate, intracellular symbiont density.

Many insects rely on intracellular bacterial symbionts to supplement their specialized diets with micronutrients. Using data from diverse and well-studied insect systems, we propose three lines of evidence suggesting that hosts have tight control over the density of their obligate, intracellular bacterial partners. First, empirical studies have demonstrated that the within-host symbiont density varies depending on the nutritional and developmental requirements of the host. Second, symbiont genomes are highly reduced and have limited capacity for self-replication or transcriptional regulation. Third, several mechanisms exist for hosts to tolerate, regulate and remove symbionts including physical compartmentalization and autophagy. We then consider whether such regulation is adaptive, by discussing the relationship between symbiont density and host fitness. We discuss current limitations of empirical studies for exploring fitness effects in host-symbiont relationships, and emphasize the potential for using mathematical models to formalize evolutionary hypotheses and to generate testable predictions for future work.

Early-life effects on body size in each sex interact to determine reproductive success in the burying beetle Nicrophorus vespilloides.

Early-life conditions have been shown to have a profound effect on an animal's body size and fecundity across diverse taxa. However, less is known about how early-life effects on fecundity within each sex interact to determine reproductive success. We used experiments with burying beetles Nicrophorus vespilloides to analyse this problem. The nutritional conditions experienced by burying beetles in early life are a key determinant of adult body size in both sexes, and adult body size in turn influences male reproductive tactics. In previous work, we showed that smaller males are more effective than larger males at stimulating virgin female fecundity. In this study, we manipulated male and female body size by restricting access to food in early development. We then conducted breeding assays, in which small and large females were mated sequentially with small and large males, and then allowed to raise offspring without paternal care. We tested whether large females, which are potentially more fecund, laid even more eggs when mated with small males. We found no evidence to support this prediction. Instead, we detected only a weak non-significant trend in the predicted direction and no equivalent trend in the number of larvae produced. However, we did find that larvae attained a greater mass by the end of development when their mother was large and mated with a small male first. We suggest that large females might have evolved counter-measures that prevent exploitation by small fecundity-stimulating males, including partial filial cannibalism. By eating surplus larvae during reproduction, larger females would leave more of the carrion for their offspring to consume. This could explain why their surviving larvae are able to attain a greater mass by the time they complete their development.

Prenatal anxiety, breastfeeding and child growth and puberty: linking evolutionary models with human cohort studies.

Background: Stress experienced by mothers during pregnancy can have both immediate and long-term effects on child development, potentially mediated by breastfeeding.Aim: Using a UK birth cohort study, we asked how maternal stress relates to breastfeeding and consequences for growth and puberty onset.Subjects and methods: We analysed data from the Avon Longitudinal Study of Parents and Children, collected via questionnaires and clinic visits (N: 698-8,506). We used reports of prenatal anxiety, breastfeeding, early growth and age at menarche or first voice change. Confounding by maternal age, parity, smoking, education and body mass index (BMI) was considered.Results: Mothers with higher levels of reported anxiety were less likely to breastfeed (Odds ratio (OR): 0.83, 95% confidence interval (CI): 0.71, 0.97). Breastfed infants had slower growth before weaning, although growth differences were unclear thereafter. Being breastfed for more than six months was associated with later puberty onset in females (2.76 months later than non-breastfed; CI: 0.9, 4.63), although the association was attenuated by confounders and BMI (1.51 months, CI: -0.38, 3.40). No association between breastfeeding and puberty onset in males was found.Conclusion: Our studies fit results shown previously, and we consider these in light of evolutionary life history theory while discussing key challenges in such an approach.

Thermal plasticity in the invasive south American tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae).

South American tomato pinworm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is a devastating invasive global insect pest of tomato, Solanum lycopersicum (Solanaceae). In nature, pests face multiple overlapping environmental stressors, which may significantly influence survival. To cope with rapidly changing environments, insects often employ a suite of mechanisms at both acute and chronic time-scales, thereby improving fitness at sub-optimal thermal environments. For T. absoluta, physiological responses to transient thermal variability remain under explored. Moreso, environmental effects and physiological responses may differ across insect life stages and this can have implications for population dynamics. Against this background, we investigated short and long term plastic responses to temperature of T. absoluta larvae (4th instar) and adults (24-48 h old) from field populations. We measured traits of temperature tolerance vis critical thermal limits [critical thermal minima (CTmin) and maxima (CTmax)], heat knockdown time (HKDT), chill coma recovery time (CCRT) and supercooling points (SCP). Our results showed that at the larval stage, Rapid Cold Hardening (RCH) significantly improved CTmin and HKDT but impaired SCP and CCRT. Heat hardening in larvae impaired CTmin, CCRT, SCP, CTmax but not HKDT. In adults, both heat and cold hardening generally impaired CTmin and CTmax, but had no effects on HKDT, SCP and CCRT. Low temperature acclimation significantly improved CTmin and HKDT while marginally compromising CCRT and CTmax, whereas high temperature acclimation had no significant effects on any traits except for HKDT in larvae. Similarly, low and high temperature acclimation had no effects on CTmin, SCPs and CTmax, while high temperature acclimation significantly compromised adult CCRT. Our results show that larvae are more thermally plastic than adults and can shift their thermal tolerance in short and long timescales. The larval plasticity reported here could be advantageous in new envirnments, suggesting an asymmetrical ecological role of larva relative to adults in facilitating T. absoluta invasion.

Adaptive Use of Information during Growth Can Explain Long-Term Effects of Early Life Experiences.

Development is a continuous process during which individuals gain information about their environment and adjust their phenotype accordingly. In many natural systems, individuals are particularly sensitive to early life experiences, even in the absence of later constraints on plasticity. Recent models have highlighted how the adaptive use of information can explain age-dependent plasticity. These models assume that information gain and phenotypic adjustments either cannot occur simultaneously or are completely independent. This assumption is not valid in the context of growth, where finding food results both in a size increase and learning about food availability. Here, we describe a simple model of growth to provide proof of principle that long-term effects of early life experiences can arise through the coupled dynamics of information acquisition and phenotypic change in the absence of direct constraints on plasticity. The increase in reproductive value from gaining information and sensitivity of behavior to experiences declines across development. Early life experiences have long-term impacts on age of maturity, yet-due to compensatory changes in behavior-our model predicts no substantial effects on reproductive success. We discuss how the evolution of sensitive windows can be explained by experiences having short-term effects on informational and phenotypic states, which generate long-term effects on life-history decisions.

Does early-life diet affect longevity? A meta-analysis across experimental studies.

Life-history theory predicts that nutrition influences lifespan owing to trade-offs between allocating resources to reproduction, growth and repair. Despite occasional reports that early diet has strong effects on lifespan, it is unclear whether this prediction is generally supported by empirical studies. We conducted a meta-analysis across experimental studies manipulating pre- or post-natal diet and measuring longevity. We found no overall effect of early diet on lifespan. We used meta-regression, considering moderator variables based on experimental and life-history traits, to test predictions regarding the strength and direction of effects that could lead to positive or negative effects. Pre-natal diet manipulations reduced lifespan, but there were no effects of later diet, manipulation type, development mode, or sex. The results are consistent with the prediction that early diet restriction disrupts growth and results in increased somatic damage, which incurs lifespan costs. Our findings raise a cautionary note, however, for placing too strong an emphasis on early diet effects on lifespan and highlight limitations of measuring these effects under laboratory conditions.

When is incomplete epigenetic resetting in germ cells favoured by natural selection?

Resetting of epigenetic marks, such as DNA methylation, in germ cells or early embryos is not always complete. Epigenetic states may therefore persist, decay or accumulate across generations. In spite of mounting empirical evidence for incomplete resetting, it is currently poorly understood whether it simply reflects stochastic noise or plays an adaptive role in phenotype determination. Here, we use a simple model to show that incomplete resetting can be adaptive in heterogeneous environments. Transmission of acquired epigenetic states prevents mismatched phenotypes when the environment changes infrequently relative to generation time and when maternal and environmental cues are unreliable. We discuss how these results may help to interpret the emerging data on transgenerational epigenetic inheritance in plants and animals.

Maternal, social and abiotic environmental effects on growth vary across life stages in a cooperative mammal.

Resource availability plays a key role in driving variation in somatic growth and body condition, and the factors determining access to resources vary considerably across life stages. Parents and carers may exert important influences in early life, when individuals are nutritionally dependent, with abiotic environmental effects having stronger influences later in development as individuals forage independently. Most studies have measured specific factors influencing growth across development or have compared relative influences of different factors within specific life stages. Such studies may not capture whether early-life factors continue to have delayed effects at later stages, or whether social factors change when individuals become nutritionally independent and adults become competitors for, rather than providers of, food. Here, we examined variation in the influence of the abiotic, social and maternal environment on growth across life stages in a wild population of cooperatively breeding meerkats. Cooperatively breeding vertebrates are ideal for investigating environmental influences on growth. In addition to experiencing highly variable abiotic conditions, cooperative breeders are typified by heterogeneity both among breeders, with mothers varying in age and social status, and in the number of carers present. Recent rainfall had a consistently marked effect on growth across life stages, yet other seasonal terms only influenced growth during stages when individuals were growing fastest. Group size and maternal dominance status had positive effects on growth during the period of nutritional dependence on carers, but did not influence mass at emergence (at 1 month) or growth at independent stages (>4 months). Pups born to older mothers were lighter at 1 month of age and subsequently grew faster as subadults. Males grew faster than females during the juvenile and subadult stage only. Our findings demonstrate the complex ways in which the external environment influences development in a cooperative mammal. Individuals are most sensitive to social and maternal factors during the period of nutritional dependence on carers, whereas direct environmental effects are relatively more important later in development. Understanding the way in which environmental sensitivity varies across life stages is likely to be an important consideration in predicting trait responses to environmental change.

Linking body mass and group dynamics in an obligate cooperative breeder.

Social and environmental factors influence key life-history processes and population dynamics by affecting fitness-related phenotypic traits such as body mass. The role of body mass is particularly pronounced in cooperative breeders due to variation in social status and consequent variation in access to resources. Investigating the mechanisms underlying variation in body mass and its demographic consequences can help elucidate how social and environmental factors affect the dynamics of cooperatively breeding populations. In this study, we present an analysis of the effect of individual variation in body mass on the temporal dynamics of group size and structure of a cooperatively breeding mongoose, the Kalahari meerkat, Suricata suricatta. First, we investigate how body mass interacts with social (dominance status and number of helpers) and environmental (rainfall and season) factors to influence key life-history processes (survival, growth, emigration and reproduction) in female meerkats. Next, using an individual-based population model, we show that the models explicitly including individual variation in body mass predict group dynamics better than those ignoring this morphological trait. Body mass influences group dynamics mainly through its effects on helper emigration and dominant reproduction. Rainfall has a trait-mediated, destabilizing effect on group dynamics, whereas the number of helpers has a direct and stabilizing effect. Counteracting effects of number of helpers on different demographic rates, despite generating temporal fluctuations, stabilizes group dynamics in the long term. Our study demonstrates that social and environmental factors interact to produce individual variation in body mass and accounting for this variation helps to explain group dynamics in this cooperatively breeding population.