Experimentally increased brood size accelerates actuarial senescence and increases subsequent reproductive effort in a wild bird population

The assumption that reproductive effort decreases somatic state, accelerating ageing, is central to our understanding of life‐history variation. Maximal reproductive effort early in life is predicted to be maladaptive by accelerating ageing disproportionally, decreasing fitness. Optimality theory predicts that reproductive effort is restrained early in life to balance the fitness contribution of reproduction against the survival cost induced by the reproductive effort. When adaptive, the level of reproductive restraint is predicted to be inversely linked to the remaining life expectancy, potentially resulting in a terminal effort in the last period of reproduction. Experimental tests of the reproductive restraint hypothesis require manipulation of somatic state and subsequent investigation of reproductive effort and residual life span. To our knowledge the available evidence remains inconclusive, and hence reproductive restraint remains to be demonstrated. We modulated somatic state through a lifelong brood size manipulation in wild jackdaws and measured its consequences for age‐dependent mortality and reproductive success. The assumption that lifelong increased brood size reduced somatic state was supported: Birds rearing enlarged broods showed subsequent increased rate of actuarial senescence, resulting in reduced residual life span. The treatment induced a reproductive response in later seasons: Egg volume and nestling survival were higher in subsequent seasons in the increased versus reduced broods' treatment group. We detected these increases in egg volume and nestling survival despite the expectation that in the absence of a change in reproductive effort, the reduced somatic state indicated by the increased mortality rate would result in lower reproductive output. This leads us to conclude that the higher reproductive success we observed was the result of higher reproductive effort. Our findings show that reproductive effort negatively covaries with remaining life expectancy, supporting optimality theory and confirming reproductive restraint as a key factor underpinning life‐history variation

Testing the effect of early‐life reproductive effort on age‐related decline in a wild insect

Funding Information Leverhulme Trust Natural Environment Research Council. Grant Numbers: NE/E005403/1, NE/H02249X/1, NE/H02364X/1, NE/L003635/1, NE/R000328/1 European Union's Horizon 2020. Grant Number: CONSENT 792215Peer reviewedPublisher PD

Males and females differ in how their behaviour changes with age in wild crickets

Because females produce and lay eggs or nurture embryos, they are constrained in the timing of their investment in reproduction. Males may have more opportunity to concentrate reproductive investment earlier in life, mating with as many females as possible soon after becoming adult. This fundamental difference leads to the prediction that because males can bias allocation towards increased reproductive investment early in life, they will use up resources earlier in their lives and hence senesce faster than females. A first step towards testing this prediction is to determine whether there are between-sex differences in age-related changes in behaviour. To do this we recorded the behaviour of crickets, Gryllus campestris, in a natural population living in and around their burrows in a meadow in northern Spain. Following individuals of both sexes through their adult lives, we recorded a range of nonreproductive behaviours, including how often they moved in and out of their burrows, how long they spent at the entrance, how long they spent outside, how quickly they left a burrow after fleeing inside to escape predation and whether they fed. We found evidence for substantial age-related changes in two of the movement traits in males, but not in females. Males moved less often and spent less time outside their burrows as they aged, whereas females showed no age-related changes in either trait. Feeding was not affected by age in males, but females fed more often as they got older. Our findings are consistent with the prediction that males senesce faster than females; experiments in nature will be needed to determine whether this pattern arises from life history trade-offs between reproduction and other traits

Ectoparasite presence and brood size manipulation interact to accelerate telomere shortening in nestling jackdaws

Early‐life conditions impact fitness, but whether the combined effect of extrinsic stressors is additive or synergistic is not well known. This is a major knowledge gap because exposure to multiple stressors is frequent. Telomere dynamics may be instrumental when testing how stressors interact because many factors affect telomere shortening, and telomere shortening predicts survival. We evaluated the effect of manipulated brood size and natural infestation by the carnid fly Carnus hemapterus on nestling growth and telomere shortening of wild jackdaws (Corvus monedula). Telomere length, measured in blood using TRF, shortened on average by 264 bp, and on average, Carnus infection induced more telomere shortening. Further analyses showed that in enlarged broods, nestlings' telomeres shortened more when parasitized, while in reduced broods there was no effect of infection on telomere shortening. We conclude that there is a synergistic effect of number of siblings and Carnus infection on telomere shortening rate: blood‐sucking parasites may negatively impact telomeres by increasing cell proliferation and/or physiological stress, and coping with infection may be less successful in enlarged broods with increased sibling competition. Larger nestlings had shorter telomeres independent of age, brood manipulation or infection. Growth was independent of infestation but in enlarged broods, nestlings were lighter at fledging. Our findings indicate that (i) evaluating consequences of early‐life environmental conditions in isolation may not yield a full picture due to synergistic effects, and (ii) effects of environmental conditions may be cryptic, for example, on telomeres, with fitness consequences expressed beyond the temporal framework of the study

Comparing individual and population measures of senescence across 10 years in a wild insect population

Acknowledgements We thank L. Rodrıguez and M.C. Munoz for unconditional support,providing access to facilities including the WildCrickets study meadow.The following people contributed to video processing and data recording:Thor Veen, Carlos Rodrıguez del Valle, Alan Rees, Hannah Hudson,Jasmine Jenkin, Lauren Morse, Emma Rogan, Emelia Hiorns, Sarah Cal-low, Jamie Barnes, Chloe Mnatzaganian, Olivia Pearson, Adele James,Robin Brown, Chris Shipway, Luke Meadows and Peter Efstratiou. We also thank www.icode.co.uk for modifications to their i-catcher video recording package to optimize it for behavioral research. Michael Briga,Fernando Colchero, Dan Nussey, Andy Young, and Thor Veen made very useful comments on preliminary versions of the manuscript, and Jon Slate has been a constant partner in the development of the project. Comments from Jean-Michel Gaillard and Felix Zajitschek represented an important contribution to improve the manuscript. This work was supported bythe Natural Environment Research Council (NERC); standard grants:NE/E005403/1, NE/H02364X/1, NE/L003635/1, NE/R000328/1, andstudentships: NE/H02249X/1 (Fisher) and NE/L003635/1 (Skicko), the Leverhulme Trust and the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement CONSENT. 792215 (Boonekamp)Peer reviewedPublisher PD

The nutritional and hedonic value of food modulate sexual receptivity in Drosophila melanogaster females

Food and sex often go hand in hand because of the nutritional cost of reproduction. For Drosophila melanogaster females, this relationship is especially intimate because their offspring develop on food. Since yeast and sugars are important nutritional pillars for Drosophila, availability of these foods should inform female reproductive behaviours. Yet mechanisms coupling food and sex are poorly understood. Here we show that yeast increases female sexual receptivity through interaction between its protein content and its odorous fermentation product acetic acid, sensed by the Ionotropic odorant receptor neuron Ir75a. A similar interaction between nutritional and hedonic value applies to sugars where taste and caloric value only increase sexual receptivity when combined. Integration of nutritional and sensory values would ensure that there are sufficient internal nutrients for egg production as well as sufficient environmental nutrients for offspring survival. These findings provide mechanisms through which females may maximize reproductive output in changing environments

Local adaptation does not constrain the expression of behaviour in translocated wild crickets

Behaviour has the potential to retard evolutionary adaptation by equipping animals with the capacity to radically change their interactions with the environment without evolving. Despite this potential for plasticity, laboratory studies frequently identify among-population differences in responses to identical stimuli, suggesting that genetic adaption often reduces behavioural flexibility. However, laboratory environments are typically far removed from nature, so their relevance to the variation we might expect to see in the wild (either among environments or as a result of changes in climate) is unclear. This is a particularly acute issue in relation to behaviour because behaving in an optimal fashion requires animals to receive and process complex sensory information which may be disrupted by laboratory conditions. We translocated newly adult male field crickets, Gryllus campestris, from five high-altitude and five low-altitude populations into a single low-altitude meadow from which we had removed all naturally present males. By tagging every individual and employing a network of 140 video cameras we were able to record comprehensive behavioural information from early adulthood until death. This allowed us to directly compare the behaviour of individuals from populations known to be genetically divergent and adapted to either high or low altitudes. We found very limited evidence for an effect on behaviour of the altitudinal environment in which crickets had evolved and developed, despite the large scale of our study (>20 000h of observations of 128 males). Our findings suggests that when provided with all the environmental cues present in their natural environment, local adaptation does not lead to substantial constraints on behaviour. This supports the hypothesis that the potential flexibility of behaviour may tend to reduce selection for local adaptation

Evidence for genetic isolation and local adaptation in the field cricket Gryllus campestris

Understanding how species can thrive in a range of environments is a central challenge for evolutionary ecology. There is strong evidence for local adaptation along large‐scale ecological clines in insects. However, potential adaptation among neighbouring populations differing in their environment has been studied much less. We used RAD sequencing to quantify genetic divergence and clustering of ten populations of the field cricket Gryllus campestris in the Cantabrian Mountains of northern Spain, and an outgroup on the inland plain. Our populations were chosen to represent replicate high and low altitude habitats. We identified genetic clusters that include both high and low altitude populations indicating that the two habitat types do not hold ancestrally distinct lineages. Using common‐garden rearing experiments to remove environmental effects, we found evidence for differences between high and low altitude populations in physiological and life‐history traits. As predicted by the local adaptation hypothesis, crickets with parents from cooler (high altitude) populations recovered from periods of extreme cooling more rapidly than those with parents from warmer (low altitude) populations. Growth rates also differed between offspring from high and low altitude populations. However, contrary to our prediction that crickets from high altitudes would grow faster, the most striking difference was that at high temperatures, growth was fastest in individuals from low altitudes. Our findings reveal that populations a few tens of kilometres apart have independently evolved adaptations to their environment. This suggests that local adaptation in a range of traits may be commonplace even in mobile invertebrates at scales of a small fraction of species' distributions

Canalisation in the wild:Effects of developmental conditions on physiological traits are inversely linked to their association with fitness

Ecological conditions affect fitness, but mechanisms causing such effects are not well known, while evolved responses to environmental variation may depend on the underlying mechanisms. Consequences of environmental conditions vary strongly between traits, but a framework to interpret such variation is lacking. We propose that variation in trait response may be explained by differential canalisation, with traits with larger fitness effects showing weaker responses to environmental perturbations due to preferential resource allocation to such traits. We tested the canalisation hypothesis using brood size manipulation in wild jackdaw nestlings in which we measured eight physiological traits (mainly oxidative stress markers), and two feather traits. For each trait, we estimated manipulation response and association with fitness (over-winter survival). As predicted, a strong negative correlation emerged between manipulation response and association with fitness (r = -0.76). We discuss the consequences of differential trait canalisation for the study of mechanisms mediating environmental effects on fitness

Data from: Canalisation in the wild: effects of developmental conditions on physiological traits are inversely linked to their association with fitness

Ecological conditions affect fitness, but mechanisms causing such effects are not well known, while evolved responses to environmental variation may depend on the underlying mechanisms. Consequences of environmental conditions vary strongly between traits, but a framework to interpret such variation is lacking. We propose that variation in trait response may be explained by differential canalisation, with traits with larger fitness effects showing weaker responses to environmental perturbations due to preferential resource allocation to such traits. We tested the canalisation hypothesis using brood size manipulation in wild jackdaw nestlings in which we measured eight physiological traits (mainly oxidative stress markers), and two feather traits. For each trait, we estimated manipulation response and association with fitness (over-winter survival). As predicted, a strong negative correlation emerged between manipulation response and association with fitness (r=-0.76). We discuss the consequences of differential trait canalization for the study of mechanisms mediating environmental effects on fitness