RESUMEN
Explaining the evolution of primate social organization has been fundamental to understand human sociality and social evolution more broadly. It has often been suggested that the ancestor of all primates was solitary and that other forms of social organization evolved later, with transitions being driven by various life history traits and ecological factors. However, recent research showed that many understudied primate species previously assumed to be solitary actually live in pairs, and intraspecific variation in social organization is common. We built a detailed database from primary field studies quantifying the number of social units expressing different social organizations in each population. We used Bayesian phylogenetic models to infer the probability of each social organization, conditional on several socioecological and life history predictors. Here, we show that when intraspecific variation is accounted for, the ancestral social organization of primates was inferred to be variable, with the most common social organization being pair-living but with approximately 10 to 20% of social units of the ancestral population deviating from this pattern by being solitary living. Body size and activity patterns had large effects on transitions between types of social organizations. As in other mammalian clades, pair-living is closely linked to small body size and likely more common in ancestral species. Our results challenge the assumption that ancestral primates were solitary and that pair-living evolved afterward emphasizing the importance of focusing on field data and accounting for intraspecific variation, providing a flexible statistical framework for doing so.
Asunto(s)
Conducta Animal , Conducta Social , Animales , Humanos , Filogenia , Teorema de Bayes , Primates , Evolución Biológica , MamíferosRESUMEN
It is generally believed that marsupials are more primitive than placentals mammals and mainly solitary living, representing the ancestral form of social organization of all mammals. However, field studies have observed pair and group-living in marsupial species, but no comparative study about their social evolution was ever done. Here, we describe the results of primary literature research on marsupial social organization which indicates that most species can live in pairs or groups and many show intra-specific variation in social organization. Using Bayesian phylogenetic mixed-effects models with a weak phylogenetic signal of 0.18, we found that solitary living was the most likely ancestral form (35% posterior probability), but had high uncertainty, and the combined probability of a partly sociable marsupial ancestor (65%) should not be overlooked. For Australian marsupials, group-living species were less likely to be found in tropical rainforest, and species with a variable social organization were associated with low and unpredictable precipitation representing deserts. Our results suggest that modern marsupials are more sociable than previously believed and that there is no strong support that their ancestral state was strictly solitary living, such that the assumption of a solitary ancestral state of all mammals may also need reconsideration.
Asunto(s)
Marsupiales , Animales , Filogenia , Evolución Biológica , Teorema de Bayes , Australia , MamíferosRESUMEN
Previous studies to understand the evolution of interspecific variation in mammalian social organization (SO; composition of social units) produced inconsistent results, possibly by ignoring intraspecific variation. Here we present systematic data on SO in artiodactyl populations, coding SO as solitary, pair-living, group-living, sex-specific or variable (different kinds of SOs in the same population). We found that 62% of 245 populations and 83% of species (83/100) exhibited variable SO. Using Bayesian phylogenetic mixed-effects models, we simultaneously tested whether research effort, habitat, sexual dimorphism, breeding seasonality or body size predicted the likelihood of different SOs and inferred the ancestral SO. Body size and sexual dimorphism were strongly associated with different SOs. Contingent on the small body size (737 g) and putative sexual monomorphism of the earliest fossil artiodactyl, the ancestral SO was most likely to be pair-living (probability = 0.76, 95% CI = 0-1), followed by variable (p = 0.19, 95% CI = 0-0.99). However, at body size values typical of extant species, variable SO becomes the dominant form (p = 0.74, 95% CI = 0.18-1.00). Distinguishing different kinds of 'variable' highlights transitions from SOs involving pair-living to SOs involving solitary and/or group-living with increasing body size and dimorphism. Our results support the assumption that ancestral artiodactyl was pair-living and highlight the ubiquity of intraspecific variation in SO.
Asunto(s)
Artiodáctilos/fisiología , Conducta Animal , Evolución Biológica , Animales , Teorema de Bayes , Femenino , Masculino , Filogenia , Caracteres SexualesRESUMEN
Energy is limited and must be allocated among competing life-history traits. Reproduction is considered one of the most energetically demanding life-history stages. Therefore, the amount of energy an individual invests in reproduction might carry fitness costs through reduced energy allocation to other activities such as health maintenance. We investigated whether reproduction impacts health in the seasonally breeding African striped mouse (Rhabdomys pumilio). We measured health in individuals that reproduced (breeders) and individuals that did not reproduce (their adult offspring) and tested whether: (1) breeders' health before reproduction was similar to that of their offspring (representing a baseline); (2) breeders' health deteriorated after reproduction; (3) breeders' health after reproduction was worse than that of their offspring. We collected blood samples from 12 breeding females and 11 breeding males both at the onset and at the end of the breeding season and from 12 adult daughters and 11 adult sons that did not reproduce at the end of the breeding season. Health was assessed using serum biochemistry analysis with VetScan Abaxis. Breeders differed considerably in their health before and after reproduction, particularly in parameters associated with digestion (lower amylase in males), metabolism (lower albumin, alkaline phosphatase, creatinine and glucose), osmoregulation (lower potassium and phosphorous in females) and immunity (higher globulin and altered alanine aminotransferase). Our results suggest that with the onset of breeding striped mice shifted their energy allocation from maintaining health to reproduction, indicating that investment into reproduction carries significant health costs.
Asunto(s)
Murinae/fisiología , Reproducción/fisiología , Factores de Edad , Alanina Transaminasa/sangre , Amilasas/sangre , Animales , Análisis Químico de la Sangre , Femenino , Tamaño de la Camada , Masculino , Estaciones del Año , SudáfricaRESUMEN
An individual's ability to survive harsh conditions might depend on its available energy, and also on its health, which is expected to decline as conditions deteriorate. Yet, we know little about how health and energy expenditure are shaped by harsh environmental conditions in free-living vertebrates. Here, we studied how African striped mice (Rhabdomys pumilio) that survived summer droughts differed in their energy expenditure and health from non-survivors. Specifically, we tested whether: (1) survivors' and non-survivors' health and energy expenditure differed before environmental conditions declined; (2) non-survivors were in poorer health and had greater energy expenditure than survivors when conditions were harshest; (3) non-survivors' health deteriorated more than that of survivors as conditions deteriorated; and (4) survivors recovered once conditions improved. Survivors and non-survivors' health was assessed using VetsScan ABAXIS, while energy expenditure was measured as resting metabolic rate (RMR). Before conditions declined, non-survivors had lower energy stores and higher globulin levels than survivors. As conditions became harsher, survivors' and non-survivors' health deteriorated but only non-survivors showed signs of permanent pathology (increased glucose and decreased globulin). Once conditions improved, survivors' health improved but was not fully restored (increased alanine aminotransferase and decreased globulin). Furthermore, while survivors and non-survivors had similar RMR before conditions became harsh; their levels diverged considerably when conditions deteriorated, with survivors having a decreased RMR and non-survivors having an increased RMR. Our results show that an individual's health before facing an environmental challenge and the way it regulates its RMR influences its ability to maintain homeostasis when conditions become more taxing.
Asunto(s)
Sequías , Metabolismo Energético , Murinae/fisiología , Adaptación Fisiológica , Animales , Ambiente , Femenino , Masculino , Estaciones del AñoRESUMEN
Shrews and their close relatives (order Eulipotyphla) are typically considered to be solitary. This impacts our understanding of mammalian social evolution: (i) the ancestor of mammals is believed to have been shrew-like, and even though Eulipotyphla are not more basal than other mammalian orders, this might have been one reason why the first mammals have been assumed to be solitary-living; (ii) Eulipotyphla are the third largest mammalian order, with hundreds of species entering comparative analyses. We review primary field studies reporting the social organization of Eulipotyphla, doing a literature research on 445 species. Primary literature was only available for 16 of the 445 species. We found 56% of the studied species to be social (38% were living in pairs), which is in sharp contrast to the 0.5 and 8% reported in other databases. We conclude that the available information indicates that shrews are more sociable than generally believed. An interesting alternative hypothesis is that the mammalian ancestor might have been pair-living. To understand the social evolution of mammals, comparative studies must be based on reliable and specific information, and more species of all orders must be studied in the field.
Asunto(s)
Eulipotyphla/fisiología , Animales , Conducta Animal , Femenino , Masculino , Conducta SocialRESUMEN
Sex-biased dispersal is observed in many taxa, but few studies have compared sex-biased dispersal among and within populations. We addressed the magnitude and habitat dependency of sex-biased dispersal in social African striped mice by separating group-related from population-related genetic variance to understand the contribution of each sex to deme structure. As dispersal over unoccupied habitat is likely to be more costly than dispersal within a population, we predicted that individuals leaving the natal population have a lower body condition, being inferior to heavier territorial individuals. Fine-scale genetic structure was detected in both sexes. Female relatedness decreased continuously from R = 0.21 at 25 m to zero at 500 m. Maximum male relatedness R = 0.05 was constant at distances between 25 and 75 m, becoming zero at 100 m. Genetic variance (F(ST) ) among seven locations was significantly higher in females than in males, while inbreeding estimates (F(IS) ) were significantly higher in males than in females. Assignment tests estimated significantly more migrants among males, while Bayesian clustering estimated only a single genetic unit cluster for males among the seven locations. The mean body mass of migrant males (44 g) was significantly lower than for males that remained resident and thus dispersed within their sub-population (48 g). Combined, the results showed habitat-independent male-biased dispersal and high female philopatry, and suggested that body condition was more important than kinship in male dispersal decisions. We suggest that locally inferior males are important for gene flow between sub-populations. Thus, males might follow alternative dispersal tactics.
Asunto(s)
Flujo Génico , Variación Genética , Genética de Población , Murinae/genética , Conducta Sexual Animal , Animales , Teorema de Bayes , Tamaño Corporal , Ecosistema , Femenino , Heterocigoto , Endogamia , Masculino , Ratones , Análisis de Secuencia de ADN , SudáfricaRESUMEN
Testis size has been related to the mating system of both vertebrates and invertebrates. These differences are regarded as adaptive responses to sperm competition in promiscuously mating species. However, not all variation in testis size can be explained by sperm competition. Here, we test the hypothesis that the evolution of large testes occurs when synchronously breeding females must be fertilized within a short period of time to avoid reproductive competition among the females. African striped mouse (Rhabdomys pumilio) males of a polygynous population with cooperative breeding and high risk of sperm depletion had testes and cauda epididymis twice as large as those of males of four different promiscuous populations with high risk of sperm competition. When paired with three females simultaneously in captivity, males of the polygynous population bred with three females within 8 days, leading to synchronous births in their harems, thereby potentially reducing the risk of infanticide. Males from the promiscuous population reproduced with only one or two females within 8 days, and births were not synchronous. We conclude that large testes are selected for in species with synchronously mating females, which is ultimately beneficial for the evolution of cooperative breeding.
Asunto(s)
Conducta Cooperativa , Sincronización del Estro/fisiología , Murinae/fisiología , Conducta Sexual Animal/fisiología , Espermatozoides/metabolismo , Testículo/anatomía & histología , Animales , Evolución Biológica , Eficiencia , Femenino , Masculino , Ratones , Murinae/metabolismo , Tamaño de los Órganos , Testículo/metabolismoRESUMEN
Goeldi's monkey (Callimico goeldii) is closely related to marmosets and tamarins. Like marmosets and tamarins, C. goeldii lives in family groups, and fathers and older offspring (helpers) participate in infant carrying. In contrast to the typical twin births in marmosets and tamarins, C. goeldii has only single offspring, and paternal carrying is delayed. We studied infant carrying following 26 births in eight groups of C. goeldii, testing hypotheses proposed in the literature on infant carrying in marmosets and tamarins. The infant was carried exclusively by the mother for the first 26.3 days after birth. Afterwards other group members participated in infant carrying. Whereas the C. goeldii mother is always the main carrier, the father does not always carry more than helpers. In contrast to other callitrichids, age and sex of sibling helpers was not found to have an effect on the participation in infant carrying. The participation in infant carrying in Callimico indicated intraindividual consistency, i.e., the amount of infant carrying performed by fathers and helpers following one birth correlated significantly with the amount of infant carrying of the same individuals following the next birth. We found a significant negative correlation between parental infant carrying and group size, indicating that helpers really do help, sharing the carrying burden with their parents. This is attributed to a clear trend for a reduction in maternal carrying in the presence of helpers, whereas fathers did not benefit from helpers. We conclude that the infant-carrying pattern in C. goeldii is different from the infant-carrying pattern in marmosets and tamarins. The main differences were that the mother instead of the father is the main carrier, and that there is a clear time delay between infant birth and when the father and helpers participate in infant carrying.