The Evolution of Primate Societies - Chapter 3

Compared with other primates, New World monkeys display relatively limited ecological variability. New World monkey anatomy and social systems, however, are extremely diverse. Several unique morphological features (e.g., claws, prehensile tails) and uncommon patterns of social organization (e.g., paternal care, cooperative breeding, female dispersal) have evolved in some platyrrhine species. Social organization and mating patterns include typical harem- like structures where mating is largely polygynous, and large multimale, multifemale groups with promiscuous mating and fi ssion- fusion societies. In addition, some species are socially monogamous and polyandrous. Even closely related species may exhibit strikingly different social organizations, as the example of the squirrel monkeys demonstrates (Mitchell et al. 1991; Boinski et al. 2005b). New World monkey behavior varies within species as well as between them. While the behavior of many species is known from only one study site, intriguing patterns of intraspecific variation are beginning to emerge from observations of populations that sometimes live in close proximity. For example, spider monkeys are often described as showing sex- segregated ranging behavior. Several studies show that males range farther, travel faster, and use larger areas than females, who tend to restrict their habitual ranging to smaller core areas within a group’s large territory (Symington 1988; Chapman 1990; Shimooka 2005). In at least one well- studied population in Yasuní National Park, Ecuador, however, males and females both travel over the entire community home range, and different females within the community show little evidence of occupying distinct core areas (Spehar et al. 2010). Similarly, in most well- studied populations of spider monkeys, females disperse and the resident males within a group are presumed to be close relatives—a suggestion corroborated by genetic data for one local population of spider monkeys in Yasuní. Still, in a different local population, males are not closely related to one another, an unexpected pattern if signifi cant male philopatry were common (Di Fiore 2009; Di Fiore et al. 2009). While the causes of this local variation in group genetic structure are not clear, it may be signifi cant that the groups examined likely had different histories of contact with humans. For longlived animals who occupy relatively small social groups, the loss of even a handful of individuals to hunting, or to any other demographic disturbance, can have a dramatic impact on a group’s genetic structure. Intragroup social relationships, in turn, are likely to be infl uenced by patterns of intragroup relatedness and by the relative availability of social partners of different age or sex class (chapter 21, this volume). Thus, historical and demographic contingencies are likely to create conditions where considerable local, intrapopulation variation in social systems exists. Slight changes in ecological conditions may also contribute to variation in the behavior of individuals living in a single population over time. For example, some authors have hypothesized that howler monkey populations may undergo dramatic fluctuations in size and composition in response to several ecological factors, including resource abundance, parasite and predation pressure, and climate (Milton 1982; Crockett & Eisenberg 1986; Crockett 1996; Milton 1996; Rudran & Fernandez- Duque 2003). This variability, not only among populations, but also within populations across time highlights the need for long- term studies. In sum, our understanding of the behavior of New World monkeys has increased dramatically over the past 25 years. This understanding highlights how their behavior varies within populations over time and among populations or species across space. As our knowledge of platyrrhine behavior continues to unfold and is enriched via additional long- term studies, a central challenge will be to explain how these variations arise. It will be important to entertain adaptive explanations while acknowledging that some differences may emerge via stochastic changes in demography (Struhsaker 2008) or nongenetic, relatively short- term, nonadaptive responses to sudden ecological change

Dieta, Forrajeo y Presupuesto de Tiempo en Cotoncillos (Callicebus discolor) del Parque Nacional Yasuní en la Amazonia Ecuatoriana

La subfamilia Callicebinae se encuentra representada por el género Callicebus, conocidos en Ecuador como cotoncillos o songo-songos (Tirira, 1999). La sistemática del género ha recibido importantes revisiones últimamente luego que Hershkovitz (1990) realizara una revisión taxonómica en la que llevó el número de especies de tres a 13 (Kinzey, 1981; de la Torre, 1998; Van Roosmalen et al., 2002). Actualmente, sólo dos especies del género se encuentran en Ecuador (C. lucifer y C. discolor, Van Roosmalen et al., 2002) y las mismas habitan el bosque lluvioso tropical amazónico (Extracto de la Introducción, el trabajo no tiene resumen)Fil: Carrillo Bilbao, Gabriel. Universidad Central del Ecuador; EcuadorFil: Di Fiore, Anthony. University of Texas at Austin; Estados UnidosFil: Fernandez Duque, Eduardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Centro de Ecología Aplicada del Litoral. Universidad Nacional del Nordeste. Centro de Ecología Aplicada del Litoral; Argentina. University of Pennsylvania; Estados Unido

Double effort: parental behavior of wild Azara's owl monkeys in the face of twins

In species of mammals that habitually bear single offspring, like most anthropoid primates, the occurrence of twins is expected to impose considerable energetic costs on the caretakers. The question then arises of how caregivers cope with the potentially increased costs of raising twins. These increased costs should lead to differing developmental rates in twins when compared to singletons, and/or to changes in the caregivers' behavior. Likewise, time budgets of parents of singletons are expected to differ from those of adults without offspring. Additionally, if twinning was an adaptive response to favorable ecological conditions, it should be more likely in years with high food abundance. Following the birth in 2011 of two sets of twins in a wild population of pair-living Azara's owl monkeys (Aotus azarae) in Northern Argentina, we used long-term demographic, behavioral, and phenological data to compare a) the proportion of time that singleton and twin infants were carried by either parent, b) adult time-budgets and ranging behavior in groups with zero, one, or two infants, and c) the availability of food in 2011 with food availability in other years. Twins, like singletons, were carried nearly exclusively by the male, and they were carried slightly more than singletons, suggesting a relatively inflexible pattern of infant care in the species. Time budgets showed that twin parents foraged more and moved less than singleton parents or groups without infants, despite the fact that phenological data indicate that fruit availability in 2011 was not substantially higher than in some of the other years. Overall, twinning thus presumably increased costs to breeders, especially males, but its effect on animals’ long-term reproductive success remains unclear.National Science Foundation (BCS-1219368); National Geographic Society (9053-11); German Science Foundation (HU1746-2 & 3); het Vreedefonds; Stichting Fundatie van de Vrijvrouwe van Renswoude te‘s-Gravenhage; Stichting Jo Kolk Studiefonds; de Stichting dr.Hendrik Muller's VaderlandschFonds; Wenner-Gren Foundation; L.S.B. Leakey Foundation; National Science Foundation (BCS- 0621020); the University of Pennsylvania Research Foundation; Zoological Society of San Dieg

Increasing biomass in Amazonian forest plots

A previous study by Phillips et al. of changes in the biomass of permanent sample plots in Amazonian forests was used to infer the presence of a regional carbon sink. However, these results generated a vigorous debate about sampling and methodological issues. Therefore we present a new analysis of biomass change in old-growth Amazonian forest plots using updated inventory data. We find that across 59 sites, the above-ground dry biomass in trees that are more than 10 cm in diameter (AGB) has increased since plot establishment by 1.22 ± 0.43 Mg per hectare per year (ha-1 yr-1), where 1 ha = 104 m2), or 0.98 ± 0.38 Mg ha-1 yr-1 if individual plot values are weighted by the number of hectare years of monitoring. This significant increase is neither confounded by spatial or temporal variation in wood specific gravity, nor dependent on the allometric equation used to estimate AGB. The conclusion is also robust to uncertainty about diameter measurements for problematic trees: for 34 plots in western Amazon forests a significant increase in AGB is found even with a conservative assumption of zero growth for all trees where diameter measurements were made using optical methods and/or growth rates needed to be estimated following fieldwork. Overall, our results suggest a slightly greater rate of net stand-level change than was reported by Phillips et al. Considering the spatial and temporal scale of sampling and associated studies showing increases in forest growth and stem turnover, the results presented here suggest that the total biomass of these plots has on average increased and that there has been a regional-scale carbon sink in old-growth Amazonian forests during the previous two decades

Increasing dominance of large lianas in Amazonian forests

Ecological orthodoxy suggests that old-growth forests should be close to dynamic equilibrium, but this view has been challenged by recent findings that neotropical forests are accumulating carbon and biomass, possibly in response to the increasing atmospheric concentrations of carbon dioxide. However, it is unclear whether the recent increase in tree biomass has been accompanied by a shift in community composition. Such changes could reduce or enhance the carbon storage potential of old-growth forests in the long term. Here we show that non-fragmented Amazon forests are experiencing a concerted increase in the density, basal area and mean size of woody climbing plants (lianas). Over the last two decades of the twentieth century the dominance of large lianas relative to trees has increased by 1.7–4.6% a year. Lianas enhance tree mortality and suppress tree growth, so their rapid increase implies that the tropical terrestrial carbon sink may shut down sooner than current models suggest. Predictions of future tropical carbon fluxes will need to account for the changing composition and dynamics of supposedly undisturbed forests

Global Conservation Significance of Ecuador's Yasuní National Park

Margot S. Bass is with Finding Species, Matt Finer is with Save America's Forests, Clinton N. Jenkins is with Duke University and University of Maryland, Holger Kreft is with University of California San Diego, Diego F. Cisneros-Heredia is with King's College London and Universidad San Francisco de Quito, Shawn F. McCracken is with Texas State University and the TADPOLE Organization, Nigel C. A. Pitman is with Duke University, Peter H. English is with UT Austin, Kelly Swing is with Universidad San Francisco de Quito, Gorky Villa is with Finding Species, Anthony Di Fiore is with New York University, Christian C. Voigt is with Leibniz Institute for Zoo and Wildlife Research, Thomas H. Kunz is with Boston University.Background -- The threats facing Ecuador's Yasuní National Park are emblematic of those confronting the greater western Amazon, one of the world's last high-biodiversity wilderness areas. Notably, the country's second largest untapped oil reserves—called “ITT”—lie beneath an intact, remote section of the park. The conservation significance of Yasuní may weigh heavily in upcoming state-level and international decisions, including whether to develop the oil or invest in alternatives. Methodology/Principal Findings -- We conducted the first comprehensive synthesis of biodiversity data for Yasuní. Mapping amphibian, bird, mammal, and plant distributions, we found eastern Ecuador and northern Peru to be the only regions in South America where species richness centers for all four taxonomic groups overlap. This quadruple richness center has only one viable strict protected area (IUCN levels I–IV): Yasuní. The park covers just 14% of the quadruple richness center's area, whereas active or proposed oil concessions cover 79%. Using field inventory data, we compared Yasuní's local (alpha) and landscape (gamma) diversity to other sites, in the western Amazon and globally. These analyses further suggest that Yasuní is among the most biodiverse places on Earth, with apparent world richness records for amphibians, reptiles, bats, and trees. Yasuní also protects a considerable number of threatened species and regional endemics. Conclusions/Significance -- Yasuní has outstanding global conservation significance due to its extraordinary biodiversity and potential to sustain this biodiversity in the long term because of its 1) large size and wilderness character, 2) intact large-vertebrate assemblage, 3) IUCN level-II protection status in a region lacking other strict protected areas, and 4) likelihood of maintaining wet, rainforest conditions while anticipated climate change-induced drought intensifies in the eastern Amazon. However, further oil development in Yasuní jeopardizes its conservation values. These findings form the scientific basis for policy recommendations, including stopping any new oil activities and road construction in Yasuní and creating areas off-limits to large-scale development in adjacent northern Peru.The Blue Moon Fund, the Conservation, Food & Health Foundation, and the Forrest and Frances Lattner Foundation funded MF. The US National Science Foundation (Graduate Research Fellowship Program), Texas State University-Department of Biology, and TADPOLE funded SM. The US National Science Foundation, the L.S.B. Leakey Foundation, the Wenner-Gren Foundation for Anthropological Research, and Primate Conservation, Inc. funded AD. Establishment of the Tiputini Biodiversity Station supported by the US National Science Foundation–DBI-0434875 (Thomas H. Kunz, PI, with Laura M. MacLatchy, Christopher J. Schneider, and C. Kelly Swing, Co-PIs). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Biological Sciences, School o

Biodiversity of protists and nematodes in the wild nonhuman primate gut

Documenting the natural diversity of eukaryotic organisms in the nonhuman primate (NHP) gut is important for understanding the evolution of the mammalian gut microbiome, its role in digestion, health and disease, and the consequences of anthropogenic change on primate biology and conservation. Despite the ecological significance of gut-associated eukaryotes, little is known about the factors that influence their assembly and diversity in mammals. In this study, we used an 18S rRNA gene fragment metabarcoding approach to assess the eukaryotic assemblage of 62 individuals representing 16 NHP species. We find that cercopithecoids, and especially the cercopithecines, have substantially higher alpha diversity than other NHP groups. Gut-associated protists and nematodes are widespread among NHPs, consistent with their ancient association with NHP hosts. However, we do not find a consistent signal of phylosymbiosis or host-species specificity. Rather, gut eukaryotes are only weakly structured by primate phylogeny with minimal signal from diet, in contrast to previous reports of NHP gut bacteria. The results of this study indicate that gut-associated eukaryotes offer different information than gut-associated bacteria and add to our understanding of the structure of the gut microbiome.Fil: Mann, Allison E.. University of British Columbia; CanadáFil: Mazel, Florent. University of British Columbia; CanadáFil: Lemay, Matthew A.. University of British Columbia; CanadáFil: Morien, Evan. University of British Columbia; CanadáFil: Billy, Vincent. University of British Columbia; CanadáFil: Kowalewski, Miguel Martin. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Museo Argentino de Ciencias Naturales "Bernardino Rivadavia". Estación Biológica de Usos Múltiples (Sede Corrientes); ArgentinaFil: Di Fiore, Anthony. University of Texas at Austin; Estados UnidosFil: Link, Andrés. Universidad de los Andes; ColombiaFil: Goldberg, Tony L.. University of Wisconsin; Estados UnidosFil: Tecot, Stacey. University of Arizona; Estados UnidosFil: Baden, Andrea L.. City University Of New York. Hunter College; Estados UnidosFil: Gomez, Andres. University of Minnesota; Estados UnidosFil: Sauther, Michelle L.. State University of Colorado at Boulder; Estados UnidosFil: Cuozzo, Frank P.. Lajuma Research Centre; SudáfricaFil: Rice, Gillian A. O.. Dartmouth College; Estados UnidosFil: Dominy, Nathaniel J.. Dartmouth College; Estados UnidosFil: Stumpf, Rebecca. University of Illinois at Urbana; Estados UnidosFil: Lewis, Rebecca J.. University of Texas at Austin; Estados UnidosFil: Swedell, Larissa. University of Cape Town; Sudáfrica. City University of New York; Estados UnidosFil: Amato, Katherine. Northwestern University; Estados UnidosFil: Wegener Parfrey, Laura. University of British Columbia; Canad

A New Assessment of Robust Capuchin Monkey (Sapajus) Evolutionary History Using Genome-Wide SNP Marker Data and a Bayesian Approach to Species Delimitation

Robust capuchin monkeys, Sapajus genus, are among the most phenotypically diverse and widespread groups of primates in South America, with one of the most confusing and often shifting taxonomies. We used a ddRADseq approach to generate genome-wide SNP markers for 171 individuals from all putative extant species of Sapajus to access their evolutionary history. Using maximum likelihood, multispecies coalescent phylogenetic inference, and a Bayes Factor method to test for alternative hypotheses of species delimitation, we inferred the phylogenetic history of the Sapajus radiation, evaluating the number of discrete species supported. Our results support the recognition of three species from the Atlantic Forest south of the São Francisco River, with these species being the first splits in the robust capuchin radiation. Our results were congruent in recovering the Pantanal and Amazonian Sapajus as structured into three monophyletic clades, though new morphological assessments are necessary, as the Amazonian clades do not agree with previous morphology-based taxonomic distributions. Phylogenetic reconstructions for Sapajus occurring in the Cerrado, Caatinga, and northeastern Atlantic Forest were less congruent with morphology-based phylogenetic reconstructions, as the bearded capuchin was recovered as a paraphyletic clade, with samples from the Caatinga biome being either a monophyletic clade or nested with the blond capuchin monkey

Paternity alone does not predict long-term investment in juveniles by male baboons

Adult male chacma baboons (Papio hamadryas ursinus) form preferential associations, or friendships, with particular lactating females. Males exhibit high levels of affiliative contact with their friends’ infants and defend them from potentially infanticidal attacks (Palombit et al. 1997). Little is known about males’ associations with juveniles once they have passed the period of infanticidal risk. We conducted an observational, experimental, and genetic study of adult male and juvenile chacma baboons in the Moremi Reserve, Botswana. We identified preferential associations between males and juveniles and used behavioral data and a playback experiment to explore whether those associations have potential fitness benefits for juveniles. We determined whether males preferentially invest in care of their own offspring. We also determined how often males invest in care of their former friends’ offspring. The majority of juveniles exhibited preferential associations with one or two males, who had almost always been their mother’s friend during infancy. However, in only a subset of these relationships was the male the actual father, in part because many fathers died or disappeared before their offspring were weaned. Male caretakers intervened on behalf of their juvenile associates in social conflicts more often than they intervened on behalf of unconnected juveniles, and they did not appear to differentiate between genetic offspring and unrelated associates. Playbacks of juveniles’ distress calls elicited a stronger response from their caretakers than from control males. Chacma males may provide care to unrelated offspring of former friends because the costs associated with such care are low compared with the potentially high fitness costs of refusing aid to a juvenile who is a possible offspring

A polymorphism of EGFR extracellular domain is associated with progression free-survival in metastatic colorectal cancer patients receiving cetuximab-based treatment

International audienceBackground: Cetuximab, a monoclonal antibody targeting Epidermal Growth Factor Receptor (EGFR), is currently used in metastatic colorectal cancer (mCRC), but predictive factors for therapeutic response are lacking. Mutational status of KRAS and EGFR, and EGFR copy number are potential determinants of cetuximab activity.Methods: We analyzed tumor tissues from 32 EGFR-positive mCRC patients receiving cetuximab/irinotecan combination and evaluable for treatment response. EGFR copy number was quantified by fluorescence in situ hybridization (FISH). KRAS exon 1 and EGFR exons coding for extracellular regions were sequenced.Results: Nine patients experienced an objective response (partial response) and 23 were considered as nonresponders (12 with stable disease and 11 with progressive disease). There was no EGFR amplification found, but high polysomy was noted in 2 patients, both of which were cetuximab responders. No EGFR mutations were found but a variant of exon 13 (R521K) was observed in 12 patients, 11 of which achieved objective response or stable disease. Progression-free and overall survivals were significantly better in patients with this EGFR exon 13 variant. KRAS mutations were found in 14 cases. While there was a trend for an increased KRAS mutation frequency in nonresponder patients (12 mutations out of 23, 52%) as compared to responder patients (2 out of 9, 22%), authentic tumor response or long-term disease stabilization was found in KRAS mutated patients.Conclusion: This preliminary study suggests that: an increase in EGFR copy number may be associated with cetuximab response but is a rare event in CRC, KRAS mutations are associated with low response rate but do not preclude any cetuximab-based combination efficacy and EGFR exon 13 variant (R521K) may predict for cetuximab benefit