Social Mammals Research Articles

Extra-group paternity varies with proxies of relatedness in a social mammal with high inbreeding risk

Abstract Behavioral mechanisms for avoiding inbreeding are common in the natural world and are believed to have evolved as a response to the negative consequences of inbreeding. However, despite a fundamental role in fitness, we have a limited understanding of the cues that individuals use to assess inbreeding risk, as well as the extent to which individual inbreeding behavior is repeatable. We used piecewise structural equation modeling of 24 years of data to investigate the causes and consequences of within- versus extra-group paternity in banded mongooses. This cooperatively breeding mammal lives in tight-knit social groups that often contain closely related opposite-sex breeders, so inbreeding can be avoided through extra-group mating. We used molecular parentage assignments to show that, despite extra-group paternity resulting in outbred offspring, within-group inbreeding occurs frequently, with around 16% litters being moderately or highly inbred. Additionally, extra-group paternity appears to be plastic, with females mating outside of their social group according to individual proxies (age and immigration status) and societal proxies (group size and age) of within-group inbreeding risk but not in direct response to levels of within-group relatedness. While individual repeatability in extra-group paternity was relatively low, female cobreeders showed high repeatability, suggesting a strong constraint arising from the opportunities for extra-group mating. The use of extra-group paternity as an inbreeding avoidance strategy is, therefore, limited by high costs, opportunity constraints, and the limited reliability of proxies of inbreeding risk.

Identification of specific call types produced by pre-weaning gilts in response to isolation

Monitoring the vocalizations produced by livestock in commercial facilities can be used to remotely assess the arousal, and perhaps welfare, of the animals. Domestic swine is an ideal candidate for this type of assessment as it is a highly social and vocal mammal, however, a standardized description of the vocal repertoire of domestic swine has yet to be established. The objectives of this study were (1) to identify specific vocalizations produced by pre-weaning gilts in response to brief 5 min isolation from dam and natal farrowing pen using advanced acoustic analysis, and, (2) examine the relationship between such vocalizations and behaviors displayed during isolation in order to examine the potential for specific vocalizations, or “call types”, to represent different arousal levels in the animal. Vocalizations were classified according to acoustic and spectral characteristics such as peak frequency, duration, frequency range, and harmonics. Over 14,000 vocalizations across 40 gilts were analyzed and categorized into seven call types (A–G). The most frequent vocalizations identified were type E calls (squeals, 28.9 %), C calls (croaks, 21.9 %), D calls (high frequency grunts, 18.4 %), and A calls (low frequency grunts, 18 %). Call type was found to co-vary with several behavioral responses to isolation. C calls (croaks) were positively correlated (P < 0.05) to behaviors interpreted as pacing in the novel environment, while G calls (low frequency grunt variant) were positively correlated (P < 0.05) to the behaviors related to active exploration of novel environment. There were no effects of litter or sow parity on the proportion of call types produced or behaviors displayed in isolation, however, there were noticeable individual differences in vocal and behavioral responses. This study demonstrates that humans may perceive multiple call types as the same vocalization produced by gilts, and therefore, more advanced acoustic analysis is needed to create an audiogram for swine objectively. Given that gilts were observed to produce the same call types, while displaying different behavioral responses to isolation (freeze, explore, or, escape), it is difficult to narrow down the valence or arousal strength of a gilt’s response to this stress-inducing context. Future research may include physiological and/or cognitive indicators of affective state in order to refine the meaning behind each call type expressed by pre-weaning gilts in isolation.

Hemispheric Specialization for Processing the Communicative and Emotional Content of Vocal Communication in a Social Mammal, the Domestic Pig.

In humans, speech perception is lateralized, with the left hemisphere of the brain dominant in processing the communicative content and the right hemisphere dominant in processing the emotional content. However, still little is known about such a division of tasks in other species. We therefore investigated lateralized processing of communicative and emotionally relevant calls in a social mammal, the pig (Sus scrofa). Based on the contralateral connection between ears and hemispheres, we compared the behavioural and cardiac responses of 36 young male pigs during binaural and monaural (left or right) playback to the same sounds. The playback stimuli were calls of social isolation and physical restraint, whose communicative and emotional relevance, respectively, were validated prior to the test by acoustic analyses and during binaural playbacks. There were indications of lateralized processing mainly in the initial detection (left head-turn bias, indicating right hemispheric dominance) of the more emotionally relevant restraint calls. Conversely, there were indications of lateralized processing only in the appraisal (increased attention during playback to the right ear) of the more communicative relevant isolation calls. This implies differential involvement of the hemispheres in the auditory processing of vocalizations in pigs and thereby hints at similarities in the auditory processing of vocal communication in non-human animals and speech in humans. Therefore, these findings provide interesting new insight in the evolution of human language and auditory lateralization.

Reproductive adaptations to high densities in social mammals

An overview of population density control in social mammals sets the framework for examining reproductive responses to increasing population densities. We begin by honoring John B. Calhoun who played a major role, starting about 70 years ago, in correcting the conventional wisdom of the time that population control was all about adjusting mortality rates. Reproduction was considered a constant, and emigration was viewed as a component of mortality. His research was mostly on domestic and feral populations of Rattus norvegicus and Mus musculus for which he built complex arenas that could house thousands of inhabitants. In addition, he constructed elaborate living quarters in the alleyways of Baltimore. For the captive populations, he would individually mark all the inhabitants so that he could identify them and observe their behavior. Eight examples of his research publications are described. He was able to document a list of reproduction related behaviors that are the main focus of this essay, and clearly demolish the simplistic notion that reproduction is a constant. A summary of some of the major issues that encompasses the science of population growth and regulation is provided. There follows a series of 19 examples of non-Calhoun publications that cover many more species of social mammals, including humans. A comprehensive list of the many negative adaptations involving reproductive processes are documented for the 27 publications reviewed confirming that in many species reproductive constraints are non-trivial. There follows a brief discussion that attempts to create a cohesive whole for this intellectual adventure.

Azure-winged magpies\u2019 decisions to share food are contingent on the presence or absence of food for the recipient

Helping others is a key feature of human behavior. However, recent studies render this feature not uniquely human, and describe discoveries of prosocial behavior in non-human primates, other social mammals, and most recently in some bird species. Nevertheless, the cognitive underpinnings of this prosociality; i.e., whether animals take others’ need for help into account, often remain obscured. In this study, we take a first step in investigating prosociality in azure-winged magpies by presenting them with the opportunity to share highly desired food with their conspecifics i) in a situation in which these conspecifics had no such food, ii) in a situation in which they too had access to that highly desired food, and iii) in an open, base-line, situation where all had equal access to the same food and could move around freely. We find that azure-winged magpies regularly share high-value food items, preferably with, but not restricted to, members of the opposite sex. Most notably, we find that these birds, and specifically the females, seem to differentiate between whether others have food or do not have food, and subsequently cater to that lack. Begging calls by those without food seem to function as cues that elicit the food-sharing, but the response to that begging is condition-dependent. Moreover, analyses on a restricted dataset that excluded those events in which there was begging showed exactly the same patterns, raising the possibility that the azure-winged magpies might truly notice when others have access to fewer resources (even in the absence of vocal cues). This sharing behavior could indicate a high level of social awareness and prosociality that should be further investigated. Further studies are needed to establish the order of intentionality at play in this system, and whether azure-winged magpies might be able to attribute desire states to their conspecifics.

The relationship between individual phenotype and the division of labour in naked mole-rats: it's complicated.

BackgroundThe naked mole-rat (Heterocephalus glaber) is among the most social mammals on the planet, living in eusocial groups of up to 300 individuals that contain a single reproductive female and up to three reproductive males. A critical aspect of their complex social system is the division of labour that allows non-breeders to form an effective workforce. Age- or weight-based polyethisms are widely cited as explanations for how labour is divided, but evidence in support of these hypotheses has been equivocal.MethodsTo assess the extent to which individual working behaviour is determined by sex, age, weight and social rank, we studied the behaviours of 103 animals from eight captive colonies. We performed focal sampling and ran mixed-effects models to assess which factors explained variation in working behaviour during six ten-minute observation periods per individual.ResultsContrary to widely-held beliefs, we found that working behaviour did not decrease linearly with weight, although polynomial regressions indicated younger and medium-sized individuals worked most frequently, while high-ranking individuals worked for the shortest periods of time. Working behaviour and its relationship with individual characteristics also varied between colonies.ConclusionsWhile age- or size-based polyethisms may have some influence on working behaviour, we argue that other characteristics of the individual and colony are also important. In particular, the interactions of individual, social and environmental factors must be considered in order to understand the emergence and effectiveness of the division of labour that is so critical to many social organisms.

Introduction. The Evolutionary Approach to Ethics: From Animal Prosociality to Human Morality.

Evolutionary research on the biological fitness of groups has recently given a prominent value to the role that prosocial behaviors play in favoring a successful adaptation to ecological niches. Such a focus marks a paradigm shift. Early views of evolution relied on the notion of natural selection as a largely competitive mechanism for the achievement of the highest amount of resources. Today, evolutionists from different schools think that collaborative attitudes are an irremovable ingredient of biological change over time. As a consequence, a number of researchers have been attracted by evolutionary studies of human behaviors. Some think that a continuity among prosocial attitudes of human beings and other social mammals (particularly primates) can be detected, and that this fact has relevance for accounting for human morality. Others deny one or the other of these claims, or both. The papers in the present special issue address how these topics impact ethics and religion.

C-low threshold mechanoafferent targeted dynamic touch modulates stress resilience in rats exposed to chronic mild stress.

Affiliative tactile interactions buffer social mammals against neurobiological and behavioral effects of stress. The aim of this study was to investigate the cutaneous mechanisms underlying such beneficial consequences of touch by determining whether daily stroking, specifically targeted to activate a velocity/force tuned class of low-threshold c-fiber mechanoreceptor (CLTM), confers resilience against established markers of chronic unpredictable mild stress (CMS). Adult male Sprague Dawley rats were exposed to 2weeks of CMS. Throughout the CMS protocol, some rats were stroked daily, either at CLTM optimal velocity (5cm/s) or outside the CLTM optimal range (30cm/s). A third CMS exposed group did not receive any tactile stimulation. The effect of CMS on serum corticosterone levels, anxiety- and depressive-like behaviors in these three groups was assessed in comparison to a control group of non-CMS exposed rats. While stroking did not mitigate the effects of CMS on body weight gain, CLTM optimal velocity stroking did significantly reduce CMS-induced elevations in corticosterone following an acute forced-swim. Rats receiving CLTM optimal stroking also showed significantly fewer anxiety-like behaviors (elevated plus-maze) than the other CMS exposed rats. In terms of depressive-like behavior, whereas the same velocity-specific resilience was observed in a forced-swim test and social interaction test both groups of stroked rats spent significantly less time interacting than control rats, though they also spent significantly less time in the corner than non-stroked CMS rats. Together, these findings support the theory CLTMs play a functional role in regulating the physiological condition of the body.

Dolphin movement direction recognition using contour-skeleton information

Detecting and tracking social marine mammals, including dolphins, can help to explain their social dynamics, predict their behavior, and measure the impact of human interference. The underwater environment is very special and different from the land environment: acoustic recorders are the main equipment for researchers to track dolphins at a long distance. Close-range detection of visual data is often seriously affected by the underwater environment, because the underwater environment is highly dynamic and the light source has attenuation in the deep water. Nonetheless, compared with acoustic information, visual data can provide more detailed information at low cost. The videos and images of dolphins provide researchers with great convenience in studying the body structure and social behavior of dolphins. At the same time, dolphin movement direction recognition helps researchers to learn more about dolphins through a series of accurate movement data. In this paper, we proposed an approach to detect the movement direction of dolphins effectively. First, the contours and skeletons are detected, which could reduce the impact of wrong detections significantly. And then another CNN-based model obtains the movement directions with feature images extracted from the previous steps. The experiment result shows the correctness and efficiency of the proposed method.

Horizontal disease transmission in lions from behavioural interfaces via social network analysis

The degree of relatedness and an interacting unifying central member can exacerbate disease transmission within a social group. The severity of the disease depends on the route, dose and frequency of infection. Group-living social mammals thus have the ability to exacerbate the spread of the disease. Lions Panthera leo are social carnivores with individuals interacting on a regular basis. We used observations of lion behaviours to define potential transmission routes between individuals and the likely spread of diseases in the lion population of the Kruger National Park. This allowed description of the epidemiology of bovine tuberculosis to mimic and predict the potential rate of horizontal disease transmission within lion prides. Social network analysis allowed us to identify the most important pride members and the implications of interactions with these members for spreading disease in prides. Three prides in the southern region of the Kruger National Park comprised degrees of relatedness within prides that predict variable links between pride members. The interactive behaviour of young lions with each other, a key element of learning in social mammals, play a key role in dictating contact rates that enhance disease transmission. Even so, within prides, R0 < 1 predicts that bovine tuberculosis should disappear from a pride. Persistence of the disease as noted for lions in Kruger can only realize through unlikely transmissions or through feeding on infected prey. Our results support lions as a spill-over host.

Higher sociability leads to lower reproductive success in female kangaroos.

In social mammals, social integration is generally assumed to improve females' reproductive success. Most species demonstrating this relationship exhibit complex forms of social bonds and interactions. However, female eastern grey kangaroos (Macropus giganteus) exhibit differentiated social relationships, yet do not appear to cooperate directly. It is unclear what the fitness consequences of such sociability could be in species that do not exhibit obvious forms of cooperation. Using 4 years of life history, spatial and social data from a wild population of approximately 200 individually recognizable female eastern grey kangaroos, we tested whether higher levels of sociability are associated with greater reproductive success. Contrary to expectations, we found that the size of a female's social network, her numbers of preferential associations with other females and her group sizes all negatively influenced her reproductive success. These factors influenced the survival of dependent young that had left the pouch rather than those that were still in the pouch. We also show that primiparous females (first-time breeders) were less likely to have surviving young. Our findings suggest that social bonds are not always beneficial for reproductive success in group-living species, and that female kangaroos may experience trade-offs between successfully rearing young and maintaining affiliative relationships.

Novel ultrastructural findings on cardiac mitochondria of huddling Brandt's voles in mild cold environment

Reduced ambient temperature has a damaging effect on mammalian myocardium. Huddling as a cooperative behavior has evolved in social mammals as a strategy to maximize adaptation to environmental cooling. Here, we studied the effects of huddling behavior on mitochondrial morphology, number, and function in the myocardia of Brandt's voles (Lasiopodomys brandtii) under cool environmental temperatures (15 °C). Results showed (1) mitochondrial swelling and cristae disruption in the cool huddling group (CH) and cool separated group (CS). Compared to the control group (CON, 22 °C), damaged mitochondria in the cool huddling and separated groups reached >90%; however, total number of mitochondria in the CH group was similar to that in the CON group. (2) ATP synthase activity was lowest in the CS group, whereas citrate synthetase activity was maintained among the three treatment groups. (3) Bax/bcl2 protein expression in the CH and CS groups was higher than that in the CON group, whereas DNA fragmentation, nuclear number, and caspase3 activity showed no significant differences among the three groups. (4) The protein expression levels of dynamin-related protein1 and mitochondrial fission factor were highest in the CH group. (5) Both protein expression of PINK1 and phosphorylation ratio of Parkin showed the pattern CS > CH > CON. (6) Total number of mitochondria was higher in males than in females. In general, the increased mitochondrial fission level observed in huddling voles partially counteracted the decrease in myocardial mitochondria caused by the increase in autophagy.

Why are dominant females not always showing higher reproductive success? A preregistration of a meta-analysis on social mammals

A recommendation of: Shivani, Elise Huchard, Dieter Lukas Preregistration - The effect of dominance rank on female reproductive success in social mammals https://github.com/dieterlukas/FemaleDominanceReproduction_MetaAnalysis/blob/trunk/Preregistration_MetaAnalysis_RankSuccess.Rmd

Competitive ability determines coalition participation and partner selection during maturation in wild male chimpanzees (Pan troglodytes schweinfurthii).

Social mammals often live in groups in which a dominance hierarchy is an important determinant of access to mates. In addition to competing individually, males may form coalitions of two or more to attack or intimidate rivals. Coalition formation could be particularly advantageous for adolescent males by helping them compensate for their physical and social immaturity. However, adolescents may struggle to attract effective coalition partners because of these inadequacies. Here, we examine the behavior of maturing male chimpanzees to test whether coalitions are more frequent among more or less powerful individuals. Our longitudinal study followed 18 males (ages 5 through 25 years) and utilized 1517 coalitions across 12 years of observation of the Kanyawara chimpanzee community in Kibale National Park, Uganda. We found that rates of coalition formation increased across maturation and that this increase was independent of a rise in the overall use of aggression. Juveniles formed coalitions almost exclusively with their mothers, while adolescents partnered primarily with peers and adult males. When adolescents and adult males formed coalitions with each other, the adolescents were more likely to join the adults than vice versa. Finally, adolescents engaged in joint behavior with adult males more often in non-aggressive vocal displays than in aggressive coalitions. Taken together, our results suggest that adolescent males are largely unable to attract the most powerful coalition partners and that they "make the best of a bad job" by joining adult males in less competitive situations, when the risk of receiving aggression from opponents is lower.

Dominance rank but not body size influences female reproductive success in mountain gorillas.

According to life history theory, natural selection has shaped trade-offs for allocating energy among growth, reproduction and maintenance to maximize individual fitness. In social mammals body size and dominance rank are two key variables believed to influence female reproductive success. However, few studies have examined these variables together, particularly in long-lived species. Previous studies found that female dominance rank correlates with reproductive success in mountain gorillas (Gorilla beringei beringei), which is surprising given they have weak dominance relationships and experience seemingly low levels of feeding competition. It is not currently known whether this relationship is primarily driven by a positive correlation between rank and body size. We used the non-invasive parallel laser method to measure two body size variables (back breadth and body length) of 34 wild adult female mountain gorillas, together with long-term dominance and demography data to investigate the interrelationships among body size, dominance rank and two measures of female reproductive success (inter-birth interval N = 29 and infant mortality N = 64). Using linear mixed models, we found no support for body size to be significantly correlated with dominance rank or female reproductive success. Higher-ranking females had significantly shorter inter-birth intervals than lower-ranking ones, but dominance rank was not significantly correlated with infant mortality. Our results suggest that female dominance rank is primarily determined by factors other than linear body dimensions and that high rank provides benefits even in species with weak dominance relationships and abundant year-round food resources. Future studies should focus on the mechanisms behind heterogeneity in female body size in relation to trade-offs in allocating energy to growth, maintenance and lifetime reproductive success.

Social animals need connection

Social Environment Much research over the past decade or so has revealed that health and lifespan in humans, highly social animals, are reduced with social adversity. We humans are not the only animals that are social, however, and similar research has shown that other social mammals are similarly influenced by isolation and adversity. Snyder-Mackler et al. reviewed the relationships between social environment and many aspects of health and well-being across nonhuman mammals and investigated the similarities between these and patterns in humans. They found many of the same threats and responses across social mammals. Science , this issue p. [eaax9553][1] [1]: /lookup/doi/10.1126/science.aax9553

Social determinants of health and survival in humans and other animals.

The social environment, both in early life and adulthood, is one of the strongest predictors of morbidity and mortality risk in humans. Evidence from long-term studies of other social mammals indicates that this relationship is similar across many species. In addition, experimental studies show that social interactions can causally alter animal physiology, disease risk, and life span itself. These findings highlight the importance of the social environment to health and mortality as well as Darwinian fitness-outcomes of interest to social scientists and biologists alike. They thus emphasize the utility of cross-species analysis for understanding the predictors of, and mechanisms underlying, social gradients in health.

Contrasts in kinship structure in mammalian societies

AbstractComparative studies of mammals confirm Hamilton’s prediction that differences in cooperative and competitive behavior across species will be related to contrasts in kinship between group members. Although theoretical models have explored the factors affecting kinship within social groups, few have analyzed the causes of contrasts in kinship among related species. Here, we describe interspecific differences in average kinship between group members among social mammals and show that a simple mathematical model that includes the number of breeding females, male reproductive skew, and litter size successfully predicts ~95% of observed variation in average kinship between group members across a sample of mammals. Our model shows that a wide range of conditions can generate groups with low average relatedness but only a small and rather specific set of conditions are likely to generate high average levels of relatedness between their members, providing insight into the relative rarity of advanced forms of cooperation in mammalian societies.

Ecological drivers of female lion (Panthera leo) reproduction in the Kruger National Park.

The role of social cues in the reproduction of social mammals, particularly carnivores, has been thoroughly studied and documented in literature. However, environmental cues such as resources of water, food, and shelter have been identified to a lesser extent. Pregnant lions (Panthera leo) are notoriously secretive during the final stages of pregnancy and postpartum. Behavioral indicators depicted by movement patterns obtained by remote detection of collared female lions in the Kruger National Park were necessary for the monitoring of birth timing. Over the study period, eight plus a potential three parturition incidences of collared females were recorded. Of the variables measured (step length, range size, duration, prey biomass, and rainfall), range size during the month of parturition was the most indicative movement pattern of a successful birth. By backdating the potential birth month of the litters, date of conception was calculated and our results revealed a correlation between the birthing peaks of preferred prey during the month of conception. Birth timing in conjunction with remote sensing and ecological factors were thus identified behaviors associated with denning.

Kinship Without Words

This article seeks to identify at what point in hominid evolution language would have become adaptive. It starts by recalling the distinction between kin-selected altruism and reciprocal altruism, noting that the former is characteristic of social insects while the latter is found among some species of social mammal. Reciprocal altruism depends on the exchange of information assuring partners of the other’s continued friendly intent, as in the iterated prisoner’s dilemma. The article focuses on species that practice “fission–fusion”: social behaviour, where the alternation between larger and smaller parties creates greater uncertainty as to individuals’ continued commitment to reciprocity. The greatest uncertainty arises in “atomistic” fission–fusion, where individuals leave and join foraging groups independently. Chimpanzees, bonobos, and human hunter–gatherers practice this type of social behaviour. There is less uncertainty where the smaller social unit is an extended family, as among vampire bats, chacma baboons, and savanna elephants. A comparison of the repertoire of calls and gestures among these species indicates that chimpanzees and bonobos have the largest repertoires. I then point out that, thanks to the higher proportion of meat in the diet, hunter–gatherers must live in far more dispersed communities than chimpanzees or bonobos, yet they practice more complex patterns of cooperation and reciprocity. This, I argue, created a social environment in which language became particularly adaptive. Homo heidelbergensis is identified as the key species in which language could have originated, during the transition between the Lower and Middle Paleolithic.