Andrew F. Russell

Egg investment is influenced by male attractiveness in the mallard.

Why females prefer to copulate with particular males is a contentious issue. Attention is currently focused on whether females choose males on the basis of their genetic quality, in order to produce more viable offspring. Support for this hypothesis in birds has come from studies showing that preferred males tend to father offspring of better condition or with increased survivorship. Before attributing greater offspring viability to a males heritable genetic quality, however, it is important to discount effects arising from confounding sources, including maternal effects. This has generally been addressed by comparing offspring viability from two different breeding attempts by the same female: one when offspring are sired by a preferred male, and one when offspring are sired by a less preferred male. However, here we show that individual female mallard (Anas platyrhynchos) lay larger eggs after copulating with preferred males and smaller eggs after copulating with less preferred males. As a result, females produced offspring of better body condition when paired with preferred males. After controlling for these differences in maternal investment, we found no effect of paternity on offspring condition. This shows that differences between half-sibs cannot always be attributed to paternal or maternal genetic effects.

Fitness benefits of prolonged post-reproductive lifespan in women

Most animals reproduce until they die, but in humans, females can survive long after ceasing reproduction. In theory, a prolonged post-reproductive lifespan will evolve when females can gain greater fitness by increasing the success of their offspring than by continuing to breed themselves. Although reproductive success is known to decline in old age, it is unknown whether women gain fitness by prolonging lifespan post-reproduction. Using complete multi-generational demographic records, we show that women with a prolonged post-reproductive lifespan have more grandchildren, and hence greater fitness, in pre-modern populations of both Finns and Canadians. This fitness benefit arises because post-reproductive mothers enhance the lifetime reproductive success of their offspring by allowing them to breed earlier, more frequently and more successfully. Finally, the fitness benefits of prolonged lifespan diminish as the reproductive output of offspring declines. This suggests that in female humans, selection for deferred ageing should wane when ones own offspring become post-reproductive and, correspondingly, we show that rates of female mortality accelerate as their offspring terminate reproduction.

Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats

In many animal societies, dominant individuals monopolize reproduction, but the tactics they employ to achieve this are poorly understood. One possibility is that aggressive dominants render their subordinates infertile by inducing chronic physiological “stress.” However, this hypothesis has been discarded largely for cooperatively breeding species, where reproductive monopolies are often extreme. Here we provide strong support for the stress-related suppression hypothesis in a cooperative mammal, the meerkat (Suricata suricatta). When pregnant, dominant females subject some subordinate females to escalating aggression, culminating in temporary evictions from the group. While evicted, subordinate females suffer chronic elevation of their glucocorticoid adrenal hormone levels, reproductive down-regulation (reduced pituitary sensitivity to gonadotropin-releasing hormone), reduced conception rates, and increased abortion rates. Rather than constantly harassing all subordinate females, dominants only become aggressive when pregnant themselves (when subordinate reproduction would otherwise conflict with their own) and target those females with whom reproductive conflict is most likely (older, pregnant, and more distantly related females). Our findings suggest that dominant female meerkats employ stressful evictions to suppress reproduction among their probable competitors, when attempting to breed themselves. Given the lack of evidence for stress-related suppression in other cooperative breeders to date, it is clear that social stress alone cannot account for the reproductive failure of subordinates across such societies. However, our findings raise the possibility that, in some cooperative breeders at least, dominants may employ stress-related suppression as a backup mechanism to guard against lapses in reproductive restraint by their subordinates.

Intrasexual competition and sexual selection in cooperative mammals

In most animals, the sex that invests least in its offspring competes more intensely for access to the opposite sex and shows greater development of secondary sexual characters than the sex that invests most. However, in some mammals where females are the primary care-givers, females compete more frequently or intensely with each other than males. A possible explanation is that, in these species, the resources necessary for successful female reproduction are heavily concentrated and intrasexual competition for breeding opportunities is more intense among females than among males. Intrasexual competition between females is likely to be particularly intense in cooperative breeders where a single female monopolizes reproduction in each group. Here, we use data from a twelve-year study of wild meerkats (Suricata suricatta), where females show high levels of reproductive skew, to show that females gain greater benefits from acquiring dominant status than males and traits that increase competitive ability exert a stronger influence on their breeding success. Females that acquire dominant status also develop a suite of morphological, physiological and behavioural characteristics that help them to control other group members. Our results show that sex differences in parental investment are not the only mechanism capable of generating sex differences in reproductive competition and emphasize the extent to which competition for breeding opportunities between females can affect the evolution of sex differences and the operation of sexual selection.

Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate

The widespread belief that kin selection is necessary for the evolution of cooperative breeding in vertebrates has recently been questioned. These doubts have primarily arisen because of the paucity of unequivocal evidence for kin preferences in cooperative behaviour. Using the cooperative breeding system of long–tailed tits (Aegithalos caudatus) in which kin and non–kin breed within each social unit and helpers are failed breeders, we investigated whether helpers preferentially direct their care towards kin following breeding failure. First, using observational data, we show that not all failed breeders actually become helpers, but that those that do help usually do so at the nest of a close relative. Second, we confirm the importance of kinship for helping in this species by conducting a choice experiment. We show that potential helpers do not become helpers in the absence of close kin and, when given a choice between helping equidistant broods belonging to kin and non–kin within the same social unit, virtually all helped at the nest of kin. This study provides strong evidence that kinship plays an essential role in the maintenance of cooperative breeding in this species.

Correlations between ultraviolet coloration, overwinter survival and offspring sex ratio in the blue tit

We studied the correlations between offspring sex ratio, UV coloration and overwinter survival in a population of blue tits, breeding in Gotland, Sweden, over three consecutive breeding seasons. In 2 of 3 years, we found that females paired to males with relatively brighter UV‐coloration produced a greater proportion of sons in their broods, and that this effect was significant with all 3 years combined, despite a significant year by male UV interaction. In addition, we found other correlates of sex ratio (breeding time, female age and clutch size) in some, but not all years, and some of these showed significantly different relationships with sex ratio between years. In both years for which data were available, there were indications that males with relatively brighter UV coloration, and that paired with females that produced male‐biased clutches, were more likely to survive to the next year. In addition, we also found that in both males and females, individuals produced similar sex ratios in consecutive years. Because correlations with the sex ratio may be expected to be weak, variation in results between years within the same population may be explained by low statistical power or genuine biological differences. Our results suggest that conclusions about sex ratio variation in birds should be based on multiple years. The correlations that we found in some years of this study are consistent with models of adaptive sex ratio adjustment in response to mate quality. However, careful experimental work is required to provide tests of the assumptions of these models, and should be a priority for future work.

When fecundity does not equal fitness: evidence of an offspring quantity versus quality trade-off in pre-industrial humans

Maternal fitness should be maximized by the optimal division of reproductive investment between offspring number and offspring quality. While evidence for this is abundant in many taxa, there have been fewer tests in mammals, and in particular, humans. We used a dataset of humans spanning three generations from pre-industrial Finland to test how increases in maternal fecundity affect offspring quality and maternal fitness in contrasting socio-economic conditions. For ‘resource-poor’ landless families, but not ‘resource-rich’ landowning families, maternal fitness returns diminished with increased maternal fecundity. This was because the average offspring contribution to maternal fitness declined with increased maternal fecundity for landless but not landowning families. This decline was due to reduced offspring recruitment with increased maternal fecundity. However, in landowning families, recruited offspring fecundity increased with increased maternal fecundity. This suggests that despite decreased offspring recruitment, maternal fitness is not reduced in favourable socio-economic conditions due to an increase in subsequent offspring fecundity. These results provide evidence consistent with an offspring quantity–quality trade-off in the lifetime reproduction of humans from poor socio-economic conditions. The results also highlight the importance of measuring offspring quality across their whole lifespan to estimate reliably the fitness consequences of increased maternal fecundity.

Cost minimization by helpers in cooperative vertebrates

When parents invest heavily in reproduction they commonly suffer significant energetic costs. Parents reduce the long-term fitness implications of these costs through increased foraging and reduced reproductive investment in the future. Similar behavioral modifications might be expected among helpers in societies of cooperative vertebrates, in which helping is associated with energetic costs. By using multivariate analyses and experiments, we show that in cooperative meerkats, Suricata suricatta, helping is associated with substantial short-term growth costs but limited long-term fitness costs. This association forms because individual contributions to cooperation are initially condition dependent, and, because when helpers invest heavily in cooperation, they increase their foraging rate during the subsequent nonbreeding period and reduce their level of cooperative investment in the subsequent reproductive period. These results provide a unique demonstration that despite significant short-term costs, helpers, like breeders, are able to reduce the fitness consequences of these costs through behavioral modifications.

Maternal effects in cooperative breeders: from hymenopterans to humans

The environment that an offspring experiences during its development can have lifelong consequences for its morphology, anatomy, physiology and behaviour that are strong enough to span generations. One aspect of an offsprings environment that can have particularly pronounced and long-lasting effects is that provided by its parent(s) (maternal effects). Some disciplines in biology have been quicker to appreciate maternal effects than others, and some organisms provide better model systems for understanding the causes and consequences of the maternal environment for ecology and evolution than others. One field in which maternal effects has been poorly represented, and yet is likely to represent a particularly fruitful area for research, is the field of cooperative breeding (i.e. systems where offspring are reared by carers in addition to parent(s)). Here, we attempt to illustrate the scope of cooperative breeding systems for maternal effects research and, conversely, highlight the importance of maternal effects research for understanding cooperative breeding systems. To this end, we first outline why mothers will commonly benefit from affecting the phenotype of their offspring in cooperative breeding systems, present potential strategies that mothers could employ in order to do so and offer predictions regarding the circumstances under which different types of maternal effects might be expected. Second, we highlight why a neglect of maternal strategies and the effects that they have on their offspring could lead to miscalculations of helper/worker fitness gains and a misunderstanding of the factors selecting for the evolution and maintenance of cooperative breeding. Finally, we introduce the possibility that maternal effects could have significant consequences for our understanding of both the evolutionary origins of cooperative breeding and the rise of social complexity in cooperative systems.

PROVISIONING RULES IN COOPERATIVELY BREEDING LONG-TAILED TITS AEGITHALOS CAUDATUS : AN EXPERIMENTAL STUDY

In a population of long-tailed tits Aegithalos caudatus all birds attempted to breed monogamously, but some helped to provision the nestlings of another pair if their own breeding attempt failed. An individual’s investment rules will determine the fitness consequences of helping for breeders and helpers, and the aim of this study was to examine how individual investment varied with the number of carers. Provisioning behaviour was investigated in two ways. First, observations of natural variation showed that males and females reduced their provisioning effort when aided by one helper, but showed no further reduction with additional helpers. By contrast, helpers did not adjust their provisioning effort in relation to the number of helpers at a nest. Secondly, the reaction of parents to the presence of helpers was tested experimentally by the temporary removal of helpers. Both parents significantly increased their provisioning rate when helpers were absent, and the total provisioning rate was unaffected by the manipulation. The reactions of breeders and helpers to the number of carers, and the fitness benefits for breeders and helpers are discussed.