Sociality, glucocorticoids and direct fitness in the communally rearing rodent, Octodon degus

While ecological causes of sociality (or group living) have been identified, proximate mechanisms remain less clear. Recently, close connections between sociality, glucocorticoid hormones (cort) and fitness have been hypothesized. In particular, cort levels would reflect a balance between fitness benefits and costs of group living, and therefore baseline cort levels would vary with sociality in a way opposite to the covariation between sociality and fitness. However, since reproductive effort may become a major determinant of stress responses (i.e., the cort–adaptation hypothesis), cort levels might also be expected to vary with sociality in a way similar to the covariation between sociality and fitness. We tested these expectations during three years in a natural population of the communally rearing degu, Octodon degus. During each year we quantified group membership, measured fecal cortisol metabolites (a proxy of baseline cort levels under natural conditions), and estimated direct fitness. We recorded that direct fitness decreases with group size in these animals. Secondly, neither group size nor the number of females (two proxies of sociality) influenced mean (or coefficient of variation, CV) baseline cortisol levels of adult females. In contrast, cortisol increased with per capita number of offspring produced and offspring surviving to breeding age during two out of three years examined. Together, our results imply that variation in glucocorticoid hormones is more linked to reproductive challenge than to the costs of group living. Most generally, our study provided independent support to the cort–adaptation hypothesis, according to which reproductive effort is a major determinant, yet temporally variable, influence on cort–fitness covariation.     

Burrow limitations and group living in the communally rearing rodent, Octodon degus

Group living is thought to evolve whenever individuals attain a net fitness advantage due to reduced predation risk or enhanced foraging efficiency, but also when individuals are forced to remain in groups, which often occurs during high-density conditions due to limitations of critical resources for independent breeding. The influence of ecological limitations on sociality has been studied little in species in which reproduction is more evenly shared among group members. Previous studies in the caviomorph rodent Octodon degus (a New World hystricognath) revealed no evidence that group living confers an advantage and suggest that burrow limitations influence formation of social groups. Our objective was to examine the relevance of ecological limitations on sociality in these rodents. Our 4-year study revealed no association between degu density and use of burrow systems. The frequency with which burrow systems were used by degus was not related to the quality of these structures; only in 1 of the 4 years did the frequency of burrow use decrease with decreasing abundance of food. Neither the number of females per group nor total group size (related measures of degu sociality) changed with yearly density of degus. Although the number of males within social groups was lower in 2008, this variation was not related clearly to varying density. The percentage of females in social groups that bred was close to 99% and did not change across years of varying density. Our results suggest that sociality in degus is not the consequence of burrow limitations during breeding. Whether habitat limitations contribute to variation in vertebrate social systems is discussed.     

Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies

This paper introduces a theme issue presenting the latest developments in research on the impacts of sociality on health and fitness. The articles that follow cover research on societies ranging from insects to humans. Variation in measures of fitness (i.e. survival and reproduction) has been linked to various aspects of sociality in humans and animals alike, and variability in individual health and condition has been recognized as a key mediator of these relationships. Viewed from a broad evolutionary perspective, the evolutionary transitions from a solitary lifestyle to group living have resulted in several new health-related costs and benefits of sociality. Social transmission of parasites within groups represents a major cost of group living, but some behavioural mechanisms, such as grooming, have evolved repeatedly to reduce this cost. Group living also has created novel costs in terms of altered susceptibility to infectious and non-infectious disease as a result of the unavoidable physiological consequences of social competition and integration, which are partly alleviated by social buffering in some vertebrates. Here, we define the relevant aspects of sociality, summarize their health-related costs and benefits, and discuss possible fitness measures in different study systems. Given the pervasive effects of social factors on health and fitness, we propose a synthesis of existing conceptual approaches in disease ecology, ecological immunology and behavioural neurosciences by adding sociality as a key factor, with the goal to generate a broader framework for organismal integration of health-related research.     

Behavioral and endocrine correlates of reproductive failure in social aggregations of captive wolverines (Gulo gulo)

Sociality in mammals is often viewed as a dichotomy, with sociality contrasted against solitariness. However, variation within these broad categories may have strong effects on individual fitness. For example, reproductive suppression of social subordinates is generally associated with group living, but suppression may also occur in solitary species if the behavioral and physiological processes involved can be modulated by the demographic environment. To investigate whether behavioral and physiological traits that normally are associated with group living might be latent even in a solitary species, we explored the level of sociality and investigated causes and mechanisms of reproductive failure in female wolverines Gulo gulo that experienced a highly aggregated social environment in captivity. Behaviorally, females showed low levels of aggression and intermediate levels of social interactions. Reproductive failure seemed to have been related to low social rank and to have occurred between ovulation and implantation in 13 out of 15 breeding attempts. However, three of eight females observed to mate produced offspring, indicating that no individual female fully managed to monopolize breeding. Reproductive failure was not related to elevated levels of glucocorticoid stress hormones. Rather, elevated glucocorticoid levels during the mating season were associated with successful reproduction. We suggest that social tendencies and physiological mechanisms mediating reproductive suppression may be viewed as reaction norms to the social environment. We further suggest that the social flexibility of solitary carnivores might be greater than is commonly observed, due to ecological constraints that may limit aggregation.     

First- and second-order sociality determine survival and reproduction in cooperative cichlids

Cooperative breeders serve as a model to study the evolution of cooperation, where costs and benefits of helping are typically scrutinized at the level of group membership. However, cooperation is often observed in multi-level social organizations involving interactions among individuals at various levels. Here, we argue that a full understanding of the adaptive value of cooperation and the evolution of complex social organization requires identifying the effect of different levels of social organization on direct and indirect fitness components. Our long-term field data show that in the cooperatively breeding, colonial cichlid fish Neolamprologus pulcher, both large group size and high colony density significantly raised group persistence. Neither group size nor density affected survival at the individual level, but they had interactive effects on reproductive output; large group size raised productivity when local population density was low, whereas in contrast, small groups were more productive at high densities. Fitness estimates of individually marked fish revealed indirect fitness benefits associated with staying in large groups. Inclusive fitness, however, was not significantly affected by group size, because the direct fitness component was not increased in larger groups. Together, our findings highlight that the reproductive output of groups may be affected in opposite directions by different levels of sociality, and that complex forms of sociality and costly cooperation may evolve in the absence of large indirect fitness benefits and the influence of kin selection.     

Hamilton's rule and the causes of social evolution

Hamilton''s rule is a central theorem of inclusive fitness (kin selection) theory and predicts that social behaviour evolves under specific combinations of relatedness, benefit and cost. This review provides evidence for Hamilton''s rule by presenting novel syntheses of results from two kinds of study in diverse taxa, including cooperatively breeding birds and mammals and eusocial insects. These are, first, studies that empirically parametrize Hamilton''s rule in natural populations and, second, comparative phylogenetic analyses of the genetic, life-history and ecological correlates of sociality. Studies parametrizing Hamilton''s rule are not rare and demonstrate quantitatively that (i) altruism (net loss of direct fitness) occurs even when sociality is facultative, (ii) in most cases, altruism is under positive selection via indirect fitness benefits that exceed direct fitness costs and (iii) social behaviour commonly generates indirect benefits by enhancing the productivity or survivorship of kin. Comparative phylogenetic analyses show that cooperative breeding and eusociality are promoted by (i) high relatedness and monogamy and, potentially, by (ii) life-history factors facilitating family structure and high benefits of helping and (iii) ecological factors generating low costs of social behaviour. Overall, the focal studies strongly confirm the predictions of Hamilton''s rule regarding conditions for social evolution and their causes.     

Temperature fluctuations during development reduce male fitness and may limit adaptive potential in tropical rainforest Drosophila

Understanding the potential for organisms to tolerate thermal stress through physiological or evolutionary responses is crucial given rapid climate change. Although climate models predict increases in both temperature mean and variance, such tolerances are typically assessed under constant conditions. We tested the effects of temperature variability during development on male fitness in the rainforest fly Drosophila birchii, by simulating thermal variation typical of the warm and cool margins of its elevational distribution, and estimated heritabilities and genetic correlations of fitness traits. Reproductive success was reduced for males reared in warm (mean 24 °C) fluctuating (±3 °C) vs. constant conditions but not in cool fluctuating conditions (mean 17 °C), although fluctuations reduced body size at both temperatures. Male reproductive success under warm fluctuating conditions was similar to that at constant 27 °C, indicating that briefly exceeding critical thermal limits has similar fitness costs to continuously stressful conditions. There was substantial heritable variation in all traits. However, reproductive success traits showed no genetic correlation between treatments reflecting temperature variation at elevational extremes, which may constrain evolutionary responses at these ecological margins. Our data suggest that even small increases in temperature variability will threaten tropical ectotherms living close to their upper thermal limits, both through direct effects on fitness and by limiting their adaptive potential.     

Social personality trait and fitness

Several recent studies have explored various aspects of animal personality and their ecological consequences. However, the processes responsible for the maintenance of personality variability within a population are still largely unknown. We have recently demonstrated that social personality traits exist in the common lizard (Lacerta vivipara) and that the variation in sociability provides an explanation for variable dispersal responses within a given species. However, we need to know the fitness consequences of variation in sociability across environmental contexts in order to better understand the maintenance of such variation. In order to achieve this, we investigated the relationship between sociability and survival, body growth and fecundity, in one-year-old individuals in semi-natural populations with varying density. 'Asocial' and 'social' lizards displayed different fitness outcomes in populations of different densities. Asocial lizards survived better in low-density populations, while social females reproduced better. Spatiotemporal variation in environmental conditions might thus be the process underlying the maintenance of these personality traits within a population. Finally, we also discuss the position of sociability in a more general individual behavioural pattern including boldness, exploration and aggressiveness.     

The influence of multiple inseminations and multiple foundresses on social evolution

The breeding biology of a population determines the way in which individuals are distributed within and between progeny groups and, thus, affects the genetic variation within and between these groups. The breeding biology of any organism can be characterized by the distribution of the numbers of mates of females, the apportionment of paternity among males, the distribution of the numbers of females reproducing in common nests, and the apportionment of total fecundity within a nest among founding females. In addition, the possibility of genetic correlations among mates or among founding females is an important consideration and will be addressed in a later paper. The influence of the breeding biology on social evolution was evaluated by deriving the necessary conditions for the spread of genes for social behaviors and the rate of spread of these genes for populations with different breeding biologies. The first step in this derivation is to demonstrate that selection for genes determining social behavior can be represented as the covariance between gene frequency and relative fitness. Secondly, it is shown that this covariance can be formally partitioned into within and between group components. Thirdly, each covariance component is shown to be equivalent to the product of a genetic variance and a coefficient of linear regression of relative fitness on gene frequency. Lastly, specific models for the genotype fitnesses and breeding biologies are assumed and the necessary conditions for the increase in the frequency of altruistic alleles are obtained. The theory illustrates that variation in the numbers of mates per female has less of an effect on the evolution of social behaviors than does variation in the numbers of reproductive females per nest. In addition, it points out that the harmonic mean number of mates per female or of females per nest is a more useful summary statistic for characterizing populations with respect to the expected degree of evolved sociality than is the arithmetic mean.     

Evolutionary association between subterranean lifestyle and female sociality in rodents

Subterranean rodents are a good model system to examine adaptive evolution of social organization. Life underground has been proposed either to favor solitariness or, to the contrary, to promote sociality. In concordance with the first idea, most specialized diggers are solitary. However, group-living in several unrelated subterranean rodent species and especially eusociality in two genera of African mole-rats, the Bathyergidae, seem to support the second hypothesis. Thus, none of the two models is fully consistent with empirical data. Here we apply the comparative phylogenetic method to test an evolutionary correlation between fossoriality and female social strategy (solitary breeding vs breeding in group). Both characters show very strong phylogenetic signal, and we found a significant correlation between them. Subterranean lifestyle is readily acquired under female sociality. By contrast, the transition to life underground is extremely unlikely under female solitariness. Thus, not only social behavior may be affected by ecological specialization as it is widely assumed, but it can itself restrain the range of possible specializations. The rates of transition from sociality to solitariness are equal under subterranean and surface-dwelling lifestyle. Sociality loss is irreversible in subterranean lineages, unlike surface-dwelling lineages. Based on the revealed transition rates we suggest that all lineages of subterranean rodents have gone through the stage of cooperation at the beginning of their evolutionary track, whereas group-living is selected against in highly specialized diggers. An odd pattern of distribution of sociality across and within truly subterranean taxa probably derives from the influence of extrinsic factors in combination with phylogenetic inertia.     

Variable helper effects, ecological conditions, and the evolution of cooperative breeding in the acorn woodpecker

The ecological conditions leading to delayed dispersal and helping behavior are generally thought to follow one of two contrasting scenarios: that conditions are stable and predictable, resulting in young being ecologically forced to remain as helpers (extrinsic constraints and the habitat saturation hypothesis), or that conditions are highly variable and unpredictable, leading to the need for helpers to raise young, at least when conditions are poor (intrinsic constraints and the hard life hypothesis). We investigated how variability in ecological conditions influences the degree to which helpers augment breeder fitness in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus), a species in which the acorn crop, territory quality, and prior breeding experience all vary in ways that have important effects on fitness. We found that the relationship between ecological conditions and the probability that birds would remain as helpers was variable but that helpers generally yielded greater fitness benefits when ecological conditions were favorable, rather than unfavorable, for breeding. These results affirm the importance of extrinsic constraints to delayed dispersal and cooperative breeding in this species, despite its dependence on a highly variable and unpredictable acorn crop. Our findings also confirm that helpers can have very different fitness effects, depending on conditions, but that those effects are not necessarily greater when breeding conditions are unfavorable.     

The nature of nurture in a wild mammal's fitness

Genetic variation in fitness is required for the adaptive evolution of any trait but natural selection is thought to erode genetic variance in fitness. This paradox has motivated the search for mechanisms that might maintain a population''s adaptive potential. Mothers make many contributions to the attributes of their developing offspring and these maternal effects can influence responses to natural selection if maternal effects are themselves heritable. Maternal genetic effects (MGEs) on fitness might, therefore, represent an underappreciated source of adaptive potential in wild populations. Here we used two decades of data from a pedigreed wild population of North American red squirrels to show that MGEs on offspring fitness increased the population''s evolvability by over two orders of magnitude relative to expectations from direct genetic effects alone. MGEs are predicted to maintain more variation than direct genetic effects in the face of selection, but we also found evidence of maternal effect trade-offs. Mothers that raised high-fitness offspring in one environment raised low-fitness offspring in another environment. Such a fitness trade-off is expected to maintain maternal genetic variation in fitness, which provided additional capacity for adaptive evolution beyond that provided by direct genetic effects on fitness.     

Individual fitness and the effects of a changing climate on the cessation and length of the breeding period using a 34‐year study of a temperate songbird

Studies of the phenological responses of animals to climate change typically emphasize the initiation of breeding although climatic effects on the cessation and length of the breeding period may be as or more influential of fitness. We quantified links between climate, the cessation and length of the breeding period, and individual survival and reproduction using a 34‐year study of a resident song sparrow (Melospiza melodia) population subject to dramatic variation in climate. We show that the cessation and length of the breeding period varied strongly across years, and predicted female annual fecundity but not survival. Breeding period length was more influential of fecundity than initiation or cessation of breeding alone. Warmer annual temperature and drier winters and summers predicted an earlier cessation of breeding. Population density, the date breeding was initiated, a female's history of breeding success, and the number of breeding attempts initiated previously also predicted the cessation of breeding annually, indicating that climatic, population, and individual factors may interact to affect breeding phenology. Linking climate projections to our model results suggests that females will both initiate and cease breeding earlier in the future; this will have opposite effects on individual reproductive rate because breeding earlier is expected to increase fecundity, whereas ceasing breeding earlier should reduce it. Identifying factors affecting the cessation and length of the breeding period in multiparous species may be essential to predicting individual fitness and population demography. Given a rich history of studies on the initiation of breeding in free‐living species, re‐visiting those data to estimate climatic effects on the cessation and length of breeding should improve our ability to predict the impacts of climate change on multiparous species.     

Birth-death symmetry in the evolution of a social trait

Studies of the evolution of a social trait often make ecological assumptions (of population structure, life history), and thus a trait can be studied many different times with different assumptions. Here, I consider a Moran model of continuous reproduction and use an inclusive fitness analysis to investigate the relationships between fecundity or survival selection and birth-death (BD) or death-birth (DB) demography on the evolution of a social trait. A simple symmetry obtains: fecundity (respectively survival) effects under BD behave the same as survival (respectively fecundity) effects under DB. When these results are specialized to a homogeneous population, greatly simplified conditions for a positive inclusive fitness effect are obtained in both a finite and an infinite population. The results are established using the elegant formalism of mathematical group theory and are illustrated with an example of a finite population arranged in a cycle with asymmetric offspring dispersal.     

Direct fitness correlates and thermal consequences of facultative aggregation in a desert lizard

Social aggregation is a common behavioral phenomenon thought to evolve through adaptive benefits to group living. Comparing fitness differences between aggregated and solitary individuals in nature - necessary to infer an evolutionary benefit to living in groups - has proven difficult because communally-living species tend to be obligately social and behaviorally complex. However, these differences and the mechanisms driving them are critical to understanding how solitary individuals transition to group living, as well as how and why nascent social systems change over time. Here we demonstrate that facultative aggregation in a reptile (the Desert Night Lizard, Xantusia vigilis) confers direct reproductive success and survival advantages and that thermal benefits of winter huddling disproportionately benefit small juveniles, which can favor delayed dispersal of offspring and the formation of kin groups. Using climate projection models, however, we estimate that future aggregation in night lizards could decline more than 50% due to warmer temperatures. Our results support the theory that transitions to group living arise from direct benefits to social individuals and offer a clear mechanism for the origin of kin groups through juvenile philopatry. The temperature dependence of aggregation in this and other taxa suggests that environmental variation may be a powerful but underappreciated force in the rapid transition between social and solitary behavior.     

Genetic diversity at neutral and adaptive loci determines individual fitness in a long-lived territorial bird

There is compelling evidence about the manifest effects of inbreeding depression on individual fitness and populations' risk of extinction. The majority of studies addressing inbreeding depression on wild populations are generally based on indirect measures of inbreeding using neutral markers. However, the study of functional loci, such as genes of the major histocompatibility complex (MHC), is highly recommended. MHC genes constitute an essential component of the immune system of individuals, which is directly related to individual fitness and survival. In this study, we analyse heterozygosity fitness correlations of neutral and adaptive genetic variation (22 microsatellite loci and two loci of the MHC class II, respectively) with the age of recruitment and breeding success of a decimated and geographically isolated population of a long-lived territorial vulture. Our results indicate a negative correlation between neutral genetic diversity and age of recruitment, suggesting that inbreeding may be delaying reproduction. We also found a positive correlation between functional (MHC) genetic diversity and breeding success, together with a specific positive effect of the most frequent pair of cosegregating MHC alleles in the population. Globally, our findings demonstrate that genetic depauperation in small populations has a negative impact on the individual fitness, thus increasing the populations' extinction risk.     

Towards a unified theory of cooperative breeding: the role of ecology and life history re-examined

We present quantitative models that unify several adaptive hypotheses for the evolution of cooperative breeding in a single framework: the ecological constraints hypothesis, the life-history hypothesis and the benefits-of-philopatry hypothesis. Our goal is to explain interspecific variation in the occurrence of cooperative breeding in terms of interspecific variation in life-history traits and ecological conditions. We analyse two models, according to whether or not helpers can inherit their parents' territory. Major results are (i) territory inheritance always promotes cooperative breeding; (ii) if territories are not inherited, neither ecological constraints nor variation in life-history traits predict interspecific variation in cooperative breeding; and (iii) if territories are inherited, the mechanism of density regulation is crucial in determining which factors promote cooperative breeding. If density dependence acts on the probability to obtain a free territory or on the survival of dispersers, variation in ecological constraints cannot explain variation in cooperative breeding. Lower adult mortality favours helping, not because it reduces the availability of free territories, but because it enhances the direct benefits of helpers. If density dependence acts on fecundity, lower probability of obtaining a free territory and lower survival of dispersers promote cooperative breeding. In this case, lower adult mortality works against the evolution of helping. We suggest that the difference between birds and social insects in the covariance between cooperative breeding and life-history traits is due to different mechanisms of density regulation that operate in these taxa, and we explain how natural selection on habitat choice might have caused these different mechanisms to operate.     

Limited indirect fitness benefits of male group membership in a lekking species

In group living species, individuals may gain the indirect fitness benefits characterizing kin selection when groups contain close relatives. However, tests of kin selection have primarily focused on cooperatively breeding and eusocial species, whereas its importance in other forms of group living remains to be fully understood. Lekking is a form of grouping where males display on small aggregated territories, which females then visit to mate. As females prefer larger aggregations, territorial males might gain indirect fitness benefits if their presence increases the fitness of close relatives. Previous studies have tested specific predictions of kin selection models using measures such as group‐level relatedness. However, a full understanding of the contribution of kin selection in the evolution of group living requires estimating individuals' indirect fitness benefits across multiple sites and years. Using behavioural and genetic data from the black grouse (Tetrao tetrix), we show that the indirect fitness benefits of group membership were very small because newcomers joined leks containing few close relatives who had limited mating success. Males' indirect fitness benefits were higher in yearlings during increasing population density but marginally changed the variation in male mating success. Kin selection acting through increasing group size is therefore unlikely to contribute substantially to the evolution and maintenance of lekking in this black grouse population.     

The distribution of fitness effects in an uncertain world

The distribution of fitness effects (DFE) among new mutations plays a critical role in adaptive evolution and the maintenance of genetic variation. Although fitness landscape models predict several key features of the DFE, most theory to date focuses on predictable environmental conditions, while ignoring stochastic environmental fluctuations that feature prominently in the ecology of many organisms. Here, we derive an extension of Fisher's geometric model that incorporates two common effects of environmental variation: (1) nonadaptive genotype‐by‐environment interactions (G × E), in which the phenotype of a given genotype varies across environmental contexts; and (2) random fluctuation of the fitness optimum, which generates fluctuating selection. We show that both factors cause a mismatch between the DFE within single generations and the distribution of geometric mean fitness effects (averaged over multiple generations) that governs long‐term evolutionary change. Such mismatches permit strong evolutionary constraints—despite an abundance of beneficial fitness variation within single environmental contexts—and to conflicting DFE estimates from direct versus indirect inference methods. Finally, our results suggest an intriguing parallel between the genetics and ecology of evolutionary constraints, with environmental fluctuations and pleiotropy placing qualitatively similar limits on the availability of adaptive genetic variation.     

The consequences on fitness of equating family contributions: inferences from a drosophila experiment

Here we present results of a Drosophila long term experiment where we study the fitness consequences of equating the number of breeding offspring contributed per family (EC) compared to a random contribution (RC) protocol. The EC strategy slows inbreeding and drift. However, it also prevents natural selection on fecundity and limits selection on viability to that occurring within families, and this includes purge against unconditionally deleterious alleles as well as adaptation to captive conditions. We used populations maintained with 5 or 25 single mated pairs, monitored inbreeding and selection intensity, and assayed competitive and non competitive fitness, as well as fecundity and viability components, in lines maintained with or without EC. In the small lines, EC showed modest advantage for viability during the whole experiment and for fitness up to generation 15 while, in the large lines, fitness increased steadily under both strategies, and EC led in the medium term to a slight fitness disadvantage. On the light of recent theory, these results can be explained as the joint consequence of new and standing deleterious mutations undergoing drift, inbreeding and selection and of adaptation to captive conditions.