The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population.

Research in medicine and evolutionary biology suggests that the sequencing of parental investment has a crucial impact on offspring life history and health. Here, we take advantage of the synchronous birth system of wild banded mongooses to test experimentally the lifetime consequences to offspring of receiving extra investment prenatally versus postnatally. We provided extra food to half of the breeding females in each group during pregnancy, leaving the other half as matched controls. This manipulation resulted in two categories of experimental offspring in synchronously born litters: (i) 'prenatal boost' offspring whose mothers had been fed during pregnancy, and (ii) 'postnatal boost' offspring whose mothers were not fed during pregnancy but who received extra alloparental care in the postnatal period. Prenatal boost offspring lived substantially longer as adults, but postnatal boost offspring had higher lifetime reproductive success (LRS) and higher glucocorticoid levels across the lifespan. Both types of experimental offspring had higher LRS than offspring from unmanipulated litters. We found no difference between the two experimental categories of offspring in adult weight, age at first reproduction, oxidative stress or telomere lengths. These findings are rare experimental evidence that prenatal and postnatal investments have distinct effects in moulding individual life history and fitness in wild mammals. This article is part of the theme issue 'Evolutionary ecology of inequality'.

A veil of ignorance can promote fairness in a mammal society.

Rawls argued that fairness in human societies can be achieved if decisions about the distribution of societal rewards are made from behind a veil of ignorance, which obscures the personal gains that result. Whether ignorance promotes fairness in animal societies, that is, the distribution of resources to reduce inequality, is unknown. Here we show experimentally that cooperatively breeding banded mongooses, acting from behind a veil of ignorance over kinship, allocate postnatal care in a way that reduces inequality among offspring, in the manner predicted by a Rawlsian model of cooperation. In this society synchronized reproduction leaves adults in a group ignorant of the individual parentage of their communal young. We provisioned half of the mothers in each mongoose group during pregnancy, leaving the other half as matched controls, thus increasing inequality among mothers and increasing the amount of variation in offspring birth weight in communal litters. After birth, fed mothers provided extra care to the offspring of unfed mothers, not their own young, which levelled up initial size inequalities among the offspring and equalized their survival to adulthood. Our findings suggest that a classic idea of moral philosophy also applies to the evolution of cooperation in biological systems.

Oxidative stress in response to heat stress in wild caught Namaqua rock mice, Micaelamys namaquensis.

Modelling of anthropogenic induced climate suggests more frequent and severe heatwaves in the future, which are likely to result in the mass die-off of several species of organisms. Oxidative stress induced by severe heat stress has previously been associated with a reduction in animal cognitive performance, depressed reproduction and lower life expectancy. Little is known about the non-lethal consequences of species should they survive extreme heat exposure. We investigated the oxidative stress experienced by the Namaqua rock mouse, a nocturnal rodent, using two experimental heat stress protocols, a 6 hour acute heat stress protocol without access to water and a 3-day heatwave simulation with ad libitum water. Oxidative stress was determined in the liver, kidney and brain using malondialdehyde (MDA) and protein carbonyl (PC) as markers of oxidative damage, and superoxide dismutase (SOD) and total antioxidant capacity (TAC) as markers of antioxidant defence. Incubator heat stress (heat and dehydration stress) was brought about by increasing the body temperatures of animals to 39-40.8 °C for 6 hours. Following incubator heat stress, significantly higher levels of MDA were observed in the liver. Dehydration did not explain the variation in oxidative markers and is likely a combined effect of thermal and dehydration stress. Individual body mass was significantly negatively correlated to kidney SOD and lipid peroxidation. A heatwave was simulated using a temperature cycle that would naturally occur during a heatwave in the species' local habitat, with a maximal ambient temperature of 38 °C. Following the simulated heatwave, SOD activity of the kidney demonstrated significantly lowered activity suggesting oxidative stress. Current heat waves in this species have the potential of causing oxidative stress. Heat and dehydration stress following exacerbated temperatures are likely to incur significant oxidative stress in multiple tissues demonstrating the importance of water availability to allow for rehydration to prevent oxidative stress.

Are aposematic signals honest? A review.

We explore the relevance of honest signalling theory to the evolution of aposematism. We begin with a general consideration of models of signal stability, with a focus on the Zahavian costly signalling framework. Next, we review early models of signalling in the context of aposematism (some that are consistent and some inconsistent with costly honest signalling). We focus on controversies surrounding the idea that aposematic signals are handicaps in a Zahavian framework. Then, we discuss how the alignment of interests between signaller and predator influences the evolution of aposematism, highlight the distinction between qualitative and quantitative honesty and review theory and research relevant to these categories. We also review recent theoretical treatments of the evolution of aposematism that have focused on honest signalling as well as empirical research on a variety of organisms, including invertebrates and frogs. Finally, we discuss future directions for empirical and theoretical research in this area.

Resistance to oxidative stress shows low heritability and high common environmental variance in a wild bird.

Oxidative stress was recently demonstrated to affect several fitness-related traits and is now well recognized to shape animal life-history evolution. However, very little is known about how much resistance to oxidative stress is determined by genetic and environmental effects and hence about its potential for evolution, especially in wild populations. In addition, our knowledge of phenotypic sexual dimorphism and cross-sex genetic correlations in resistance to oxidative stress remains extremely limited despite important evolutionary implications. In free-living great tits (Parus major), we quantified heritability, common environmental effect, sexual dimorphism and cross-sex genetic correlation in offspring resistance to oxidative stress by performing a split-nest cross-fostering experiment where 155 broods were split, and all siblings (n = 791) translocated and raised in two other nests. Resistance to oxidative stress was measured as both oxidative damage to lipids and erythrocyte resistance to a controlled free-radical attack. Both measurements of oxidative stress showed low additive genetic variances, high common environmental effects and phenotypic sexual dimorphism with males showing a higher resistance to oxidative stress. Cross-sex genetic correlations were not different from unity, and we found no substantial heritability in resistance to oxidative stress at adult age measured on 39 individuals that recruited the subsequent year. Our study shows that individual ability to resist to oxidative stress is primarily influenced by the common environment and has a low heritability with a consequent low potential for evolution, at least at an early stage of life.

Winter food provisioning reduces future breeding performance in a wild bird.

Supplementation of food to wild birds occurs on an enormous scale worldwide, and is often cited as an exemplar of beneficial human-wildlife interaction. Recently it has been speculated that winter feeding could have negative consequences for future reproduction, for example by enabling low quality individuals to recruit into breeding populations. However, evidence that winter feeding has deleterious impacts on reproductive success is lacking. Here, in a landscape-scale study of blue tits (Cyanistes caeruleus) across multiple years, we show that winter food supplementation reduced breeding performance the following spring. Compared to unfed populations, winter-fed birds produced offspring that weighed less, were smaller, and had lower survival. This impairment was observed in parents that had received fat only, or in combination with vitamin E, suggesting some generality in the mechanism by which supplementary feeding affected reproduction. Our results highlight the potential for deleterious population-level consequences of winter food supplementation on wild birds.

Male attractiveness, fertility and susceptibility to oxidative stress are influenced by inbreeding in Drosophila simulans.

Inbreeding frequently leads to inbreeding depression, a reduction in the trait values of inbred individuals. Inbreeding depression has been documented in sexually selected characters in several taxa, and while there is correlational evidence that male fertility is especially susceptible to inbreeding depression, there have been few direct experimental examinations of this. Here, we assessed inbreeding depression in male fertility and a range of other male fitness correlates in Drosophila simulans. We found that male fertility and attractiveness were especially susceptible to inbreeding depression. Additionally, levels of testicular oxidative stress were significantly elevated in inbred males, although sperm viability did not differ between inbred and outbred males. Copulation duration, induction of oviposition, and the proportion of eggs hatching did not differ for females mated to inbred or outbred males. Nevertheless, our results clearly show that key male fitness components are impaired by inbreeding and provide evidence that aspects of male fertility are especially susceptible to inbreeding depression.

Oxidative stress and the effect of parasites on a carotenoid-based ornament.

Oxidative stress, the physiological condition whereby the production of reactive oxygen and nitrogen species overwhelms the capacity of antioxidant defences, causes damage to key bio-molecules. It has been implicated in many diseases, and is proposed as a reliable currency in the trade-off between individual health and ornamentation. Whether oxidative stress mediates the expression of carotenoid-based signals, which are among the commonest signals of many birds, fish and reptiles, remains controversial. In the present study, we explored interactions between parasites, oxidative stress and the carotenoid-based ornamentation of red grouse Lagopus lagopus scoticus. We tested whether removing nematode parasites influenced both oxidative balance (levels of oxidative damage and circulating antioxidant defences) and carotenoid-based ornamentation. At the treatment group level, parasite purging enhanced the size and colouration of ornaments but did not significantly affect circulating carotenoids, antioxidant defences or oxidative damage. However, relative changes in these traits among individuals indicated that males with a greater number of parasites prior to treatment (parasite purging) showed a greater increase in the levels of circulating carotenoids and antioxidants, and a greater decrease in oxidative damage, than those with initially fewer parasites. At the individual level, a greater increase in carotenoid pigmentation was associated with a greater reduction in oxidative damage. Therefore, an individual's ability to express a carotenoid-based ornament appeared to be linked to its current oxidative balance and susceptibility to oxidative stress. Our experimental results suggest that oxidative stress can mediate the impact of parasites on carotenoid-based signals, and we discuss possible mechanisms linking carotenoid-based ornaments to oxidative stress.

Female ornamentation and egg carotenoids of six sympatric gobies.

Belly colouration, gonad carotenoid concentration and skin transparency were quantified in gravid Gobiusculus flavescens, as well as in females of five sympatric gobies where belly ornamentation has not been described. Although G. flavescens females did, indeed, have far more colourful bellies than the other species, this could only in part be explained by a high concentration of total gonad carotenoids. Comparable, or occasionally higher, carotenoid levels were found in the gonads of other species. Instead, the unusual ornamentation of G. flavescens arises from a unique combination of carotenoid-rich gonads and a highly transparent abdominal skin.

Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment.

We investigated in the black-headed gull whether female deposition of antioxidants and immunoglobulins (enhancing early immune function), and testosterone (suppressing immune function and increasing early competitive skills) correlate suggesting that evolution has favoured the mutual adjustment of different pathways for maternal effects. We also took egg mass, the position of the egg in the laying sequence and offspring sex into account, as these affect offspring survival. Yolk antioxidant and immunoglobulin concentrations decreased across the laying order, while yolk testosterone concentrations increased. This may substantially handicap the immune defence of last-hatched chicks. The decrease in antioxidant levels was greater when mothers had a low body mass and when the increase in testosterone concentrations was relatively large. This suggests that female black-headed gulls are constrained in the deposition of antioxidants in last-laid eggs and compensate for this by enhanced testosterone deposition. The latter may be adaptive since it re-allocates the chick's investment from costly immune function to growth and competitive skills, necessary to overcome the consequences of hatching late from an egg of reduced quality.

Carotenoid discrimination by the avian embryo: a lesson from wild birds.

The concentrations (microg/g wet yolk) of total carotenoids in eggs of the common moorhen (Gallinula chloropus), American coot (Fulica americana) and lesser black-backed gull (Larus fuscus), collected in the wild, were 47.5, 131.0 and 71.6, respectively. In contrast to data for eggs of the domestic chicken, beta-carotene was a significant component in the yolks of these three wild species, forming 25-29% by wt. of the total carotenoids present. The concentration of total carotenoids in the livers of the newly-hatched chicks was 5-10 times higher than in the other tissues and beta-carotene was again a major component, forming 37-58% of the hepatic carotenoids. In the newly-hatched gull, the proportions of both lutein and zeaxanthin were very low in the liver but high in the heart and muscle when compared with the yolk. By contrast canthaxanthin, echinenone and beta-carotene were very minor constituents of heart and muscle when compared with their proportions in the yolk of the gull. The proportions of lutein and zeaxanthin in the liver of the newly-hatched coot and moorhen were also far lower than in the yolk whereas the liver was relatively enriched with beta-cryptoxanthin, beta-carotene and (in the moorhen) echinenone. The results indicate that avian embryos discriminate between different carotenoids during their distribution from the yolk to the various tissues.