Evolution of Multilevel Social Systems in Nonhuman Primates and Humans

Multilevel (or modular) societies are a distinct type of primate social system whose key features are single-male-multifemale, core units nested within larger social bands. They are not equivalent to fission-fusion societies, with the latter referring to routine variability in associations, either on an individual or subunit level. The purpose of this review is to characterize and operationalize multilevel societies and to outline their putative evolutionary origins. Multilevel societies are prevalent in three primate clades: papionins, Asian colobines, and hominins. For each clade, we portray the most parsimonious phylogenetic pathway leading to a modular system and then review and discuss likely socioecological conditions promoting the establishment and maintenance of these societies. The multilevel system in colobines (most notably Rhinopithecus and Nasalis) has likely evolved as single-male harem systems coalesced, whereas the multilevel system of papionins (Papio hamadryas, Theropithecus gelada) and hominins most likely arose as multimale-multifemale groups split into smaller units. We hypothesize that, although ecological conditions acted as preconditions for the origin of multilevel systems in all three clades, a potentially important catalyst was intraspecific social threat, predominantly bachelor threat in colobines and female coercion/infanticide in papionins and humans. We emphasize that female transfers within bands or genetic relationships among leader males help to maintain modular societies by facilitating interunit tolerance. We still lack a good or even basic understanding of many facets of multilevel sociality. Key remaining questions are how the genetic structure of a multilevel society matches the observed social effort of its members, to what degree cooperation of males of different units is manifest and contributes to band cohesion, and how group coordination, communication, and decision making are achieved. Affiliative and cooperative interunit relations are a hallmark of human societies, and studying the precursors of intergroup pacification in other multilevel primates may provide insights into the evolution of human uniquenes

Is the New Primate Genus Rungwecebus a Baboon?

BACKGROUND: In 2005, a new primate species from Tanzania, the kipunji, was described and recognized as a member of the mangabey genus Lophocebus. However, molecular investigations based upon a number of papionins, including a limited sample of baboons of mainly unknown geographic origin, identified the kipunji as a sister taxon to Papio and not as a member of Lophocebus. Accordingly, the kipunji was separated into its own monotypic genus, Rungwecebus. METHODOLOGY/PRINCIPAL FINDINGS: We compare available mitochondrial and nuclear sequence data from the voucher specimen of Rungwecebus to other papionin lineages, including a set of geographically proximal (parapatric) baboon samples. Based on mitochondrial sequence data the kipunji clusters with baboon lineages that lie nearest to it geographically, i.e. populations of yellow and chacma baboons from south-eastern Africa, and thus does not represent a sister taxon to Papio. Nuclear data support a Papio+Rungwecebus clade, but it remains questionable whether Rungwecebus represents a sister taxon to Papio, or whether it is nested within the genus as depicted by the mitochondrial phylogeny. CONCLUSIONS/SIGNIFICANCE: Our study clearly supports a close relationship between Rungwecebus and Papio and might indicate that the kipunji is congeneric with baboon species. However, due to its morphological and ecological uniqueness Rungwecebus more likely represents a sister lineage to Papio and experienced later introgressive hybridization. Presumably, male (proto-)kipunjis reproduced with sympatric female baboons. Subsequent backcrossing of the hybrids with kipunjis would have resulted in a population with a nuclear kipunji genome, but which retained the yellow/chacma baboon mitochondrial genome. Since only one kipunji specimen was studied, it remains unclear whether all members of the new genus have been impacted by intergeneric introgression or rather only some populations. Further studies with additional Rungwecebus samples are necessary to elucidate the complete evolutionary history of this newly-described primate genus

Copulation patterns in captive hamadryas baboons: a quantitative analysis

For primates, as for many other vertebrates, copulation which results in ejaculation is a prerequisite for reproduction. The probability of ejaculation is affected by various physiological and social factors, for example reproductive state of male and female and operational sex-ratio. In this paper, we present quantitative and qualitative data on patterns of sexual behaviour in a captive group of hamadryas baboons (Papio hamadryas), a species with a polygynous–monandric mating system. We observed more than 700 copulations and analysed factors that can affect the probability of ejaculation. Multilevel logistic regression analysis and Akaike’s information criterion (AIC) model selection procedures revealed that the probability of successful copulation increased as the size of female sexual swellings increased, indicating increased probability of ovulation, and as the number of females per one-male unit (OMU) decreased. In contrast, occurrence of female copulation calls, sex of the copulation initiator, and previous male aggression toward females did not affect the probability of ejaculation. Synchrony of oestrus cycles also had no effect (most likely because the sample size was too small). We also observed 29 extra-group copulations by two non-adult males. Our results indicate that male hamadryas baboons copulated more successfully around the time of ovulation and that males in large OMUs with many females may be confronted by time or energy-allocation problems

Fluctuating asymmetry and feather growth bars as biomarkers to assess the habitat quality of shade coffee farming for avian diversity conservation

Shade coffee farming has been promoted as a means of combining sustainable coffee production and biodiversity conservation. Supporting this idea, similar levels of diversity and abundance of birds have been found in shade coffee and natural forests. However, diversity and abundance are not always good indicators of habitat quality because there may be a lag before population effects are observed following habitat conversion. Therefore, other indicators of habitat quality should be tested. In this paper, we investigate the use of two biomarkers: fluctuating asymmetry (FA) of tarsus length and rectrix mass, and feather growth bars (average growth bar width) to characterize the habitat quality of shade coffee and natural forests. We predicted higher FA and narrower feather growth bars in shade coffee forest versus natural forest, indicating higher quality in the latter. We measured and compared FA in tarsus length and rectrix mass and average growth bar width in more than 200 individuals of five bird species. The extent of FA in both tarsus length and rectrix mass was not different between the two forest types in any of the five species. Similarly, we found no difference in feather growth between shade coffee and natural forests for any species. Therefore, we conclude our comparison of biomarkers suggests that shade coffee farms and natural forests provide similar habitat quality for the five species we examined

Population dynamics of the Manyara monkey (Cercopithecus mitis manyaraensis) and vervet monkey (Chlorocebus pygerythrus) in Lake Manyara National Park, Tanzania

Estimating population densities and their trends over time is essential for understanding primate ecology and for guiding conservation efforts. From 2011 through to 2019, we counted two guenon species during seasonal road transect surveys in Lake Manyara National Park: the Tanzania-endemic Manyara monkey Cercopithecus mitis manyaraensis (International Union for Conservation of Nature and Natural Resources, IUCN, Red List category of “endangered”) and the vervet monkey Chlorocebus pygerythrus (Red List category of “least concern”). To account for imperfect detectability, we analysed the data in a line distance sampling framework, fitted species-specific detection functions, and subsequently estimated seasonal densities. To test for seasonal differences and yearly trends in the species-specific density estimates, we fitted generalized additive models. Seasonal point density estimates fluctuated considerably during the 9 years (2011–2019) of our study, ranging from 3 to 29 individuals km−2 for Manyara monkeys and from 19 to 83 individuals km−2 for vervet monkeys. Densities of both taxa did not differ seasonally, and we did not detect marked directional population trends. Our study illustrates the utility and limitations of line distance sampling for long-term primate monitoring. Beyond informing primate ecology and management, our results highlight the conservation importance of Lake Manyara National Park for primate conservation.</p

Group Composition of Guinea Baboons (Papio papio) at a Water Place Suggests a Fluid Social Organization

Baboon social systems are among the most studied in primates. Solid knowledge of the hamadryas and savannah baboon systems has accumulated, leading to a dichotomic view of baboon social systems. Hamadryas baboons live in multilayered troops based on 1-male units whereas savannah baboons live in multimale multifemale groups based on a network of related females. Less attention has been paid to their West African congenerics, the Guinea baboons, Papio papio. To fill this gap, in 2007 we initiated a long-term study of a baboon troop ranging in the Niokolo Koba National Park in southeastern Senegal. Earlier studies suggested a tendency for a multilayered social system in Guinea baboons, similar to the hamadryas baboon organization. Therefore, as a first approach to analyzing variability in party size and composition, we observed members of the troop crossing an open area from a fixed point for 3 mo during the dry and wet seasons. We counted individuals and recorded changes in composition of both arriving and departing parties. Party size and composition were highly variable on both a daily and a seasonal basis; 45.9% of the arriving parties changed in composition while crossing the open area, either splitting into smaller parties or fusing into larger ones, suggesting a fluid organization. Our data support the existence of neither a hamadryas baboon-like multilayered social organization nor a stable medium-sized multimale multifemale group as in savannah baboons. In light of our data we may need to revise the dichotomic view of baboon social systems and include space for greater variability of their social systems

Mitogenomic phylogeny of the common long-tailed macaque (Macaca fascicularis fascicularis)

Background Long-tailed macaques (Macaca fascicularis) are an important model species in biomedical research and reliable knowledge about their evolutionary history is essential for biomedical inferences. Ten subspecies have been recognized, of which most are restricted to small islands of Southeast Asia. In contrast, the common long-tailed macaque (M. f. fascicularis) is distributed over large parts of the Southeast Asian mainland and the Sundaland region. To shed more light on the phylogeny of M. f. fascicularis, we sequenced complete mitochondrial (mtDNA) genomes of 40 individuals from all over the taxon’s range, either by classical PCR-amplification and Sanger sequencing or by DNA-capture and high-throughput sequencing. Results Both laboratory approaches yielded complete mtDNA genomes from M. f. fascicularis with high accuracy and/or coverage. According to our phylogenetic reconstructions, M. f. fascicularis initially diverged into two clades 1.70 million years ago (Ma), with one including haplotypes from mainland Southeast Asia, the Malay Peninsula and North Sumatra (Clade A) and the other, haplotypes from the islands of Bangka, Java, Borneo, Timor, and the Philippines (Clade B). The three geographical populations of Clade A appear as paraphyletic groups, while local populations of Clade B form monophyletic clades with the exception of a Philippine individual which is nested within the Borneo clade. Further, in Clade B the branching pattern among main clades/lineages remains largely unresolved, most likely due to their relatively rapid diversification 0.93-0.84 Ma. Conclusions Both laboratory methods have proven to be powerful to generate complete mtDNA genome data with similarly high accuracy, with the DNA-capture and high-throughput sequencing approach as the most promising and only practical option to obtain such data from highly degraded DNA, in time and with relatively low costs. The application of complete mtDNA genomes yields new insights into the evolutionary history of M. f. fascicularis by providing a more robust phylogeny and more reliable divergence age estimations than earlier studies