Little genetic information is available to evaluate hypotheses concerning the parameters that affect population genetic structure in primate taxa that exhibit interspecific variation in social ...systems, such as squirrel monkeys (
Saimiri
). Here, we used genetic data to assess dispersal patterns, kin structure, and preferential association with same-sex kin in a wild population of
Saimiri sciureus macrodon
. We also analyzed behavioral data to assess whether individuals that maintain shorter interindividual distances show increased insect foraging success. If there was greater male than female dispersal, then we expected mean pairwise relatedness,
F
ST
values, and intragroup mean corrected assignment indices to be greater among adult females than among adult males. We also expected matrices of pairwise affinity indices (PAIs) for “association” (time spent ≤5 m) and “proximity” (time spent ≤10 m) among female dyads to positively correlate with a matrix of female pairwise relatedness. Not only did we find support for female philopatry, but we also found significant positive relationships between the relatedness matrix and each of the PAI matrices: females were more likely to be associated with (and proximal to) close female relatives than more distant relatives or unrelated individuals. Foraging analyses revealed that females had higher insect capture rates than males, and this sex difference may be related to a smaller mean interindividual distance among closely related female group members. Our result shows how estimates of genetic relatedness are useful for testing predictions regarding the evolution of sex-biased dispersal patterns, as well as potential relationships between kin-biased social behaviors and foraging success.
Aim: Capuchin monkey species are widely distributed across Central and South America. Morphological studies consistently divide the clade into robust and gracile forms, which show extensive sympatry ...in the Amazon Basin. We use genetic data to test whether Miocene or Plio-Pleistocene processes may explain capuchin species' present distributions, and consider three possible scenarios to explain widespread sympatry. Location: The Neotropics, including the Amazon and Atlantic Coastal Forest. Methods: We sequenced the 12S ribosomal RNA and cytochrome b genes from capuchin monkey specimens. The majority were sampled from US museum collections and were wild-caught individuals of known provenance across their distribution. We applied a Bayesian discrete-states diffusion model, which reconstructed the most probable history of invasion across nine subregions. We used comparative methods to test for phylogeographic association and dispersal rate variation. Results: Capuchins contained two well supported monophyletic clades, the morphologically distinct 'gracile' and 'robust' groups. The time-tree analysis estimated a late Miocene divergence between Cebus and Sapajus and a subsequent Plio-Pleistocene diversification within each of the two clades. Bayesian analysis of phylogeographic diffusion history indicated that the current wide-ranging sympatry of Cebus and Sapajus across much of the Amazon Basin was the result of a single explosive late Pleistocene invasion of Sapajus from the Atlantic Forest into the Amazon, where Sapajus is now sympatric with gracile capuchins across much of their range. Main conclusions: The biogeographic history of capuchins suggests late Miocene geographic isolation of the gracile and robust forms. Each form diversified independently, but during the Pleistocene, the robust Sapajus expanded its range from the Atlantic Forest to the Amazon, where it has now encroached substantially upon what was previously the exclusive range of gracile Cebus. The genus Cebus, as currently recognized, should be split into two genera to reflect the Miocene divergence and two subsequent independent Pliocene radiations: Cebus from the Amazon and Sapajus from the Atlantic Forest.
Anecdotal reports of predation as well as observed predation attempts and rates of animal disappearance provide some of the most relevant data for evaluating the influence that predation risk may ...have on primate behavioural ecology. Here, we report rates of disappearance from six groups of red titi monkeys (Callicebus discolor) and two groups of equatorial sakis (Pithecia aequatorialis) followed over a period of four and a half years at a lowland site in Amazonian Ecuador. We also describe the first direct observation of a harpy eagle (Harpia harpyja) preying upon a titi monkey, as well as 3 unsuccessful attacks by tayras (Eira barbara) on titi monkeys and 4 unsuccessful attacks by various raptors on sakis. Our data indicate that pitheciid primates may face a wider array of possible predators than previously recognized, and that titi monkeys and sakis are susceptible to different major classes of predators. Our observations also suggest differences in the sex role during predator defence that could be related to the evolution and maintenance of monogamous systems.
With their large body size and “slow” life histories, atelin primates are thought to follow a risk‐averse breeding strategy, similar to capital breeders, in which they accumulate energy reserves in ...anticipation of future reproductive events such as gestation and lactation. However, given the paucity of longitudinal data from wild populations, few studies to date have been able to compare the timing of reproductive events (e.g., copulations, conceptions, and births) in relation to shifting resource availability over multiple years. We examined the reproductive patterns of two atelin species—white‐bellied spider monkeys (Ateles belzebuth) and lowland woolly monkeys (Lagothrix lagotricha poeppigii)—in relation to habitat‐wide estimates of fruit availability at the Tiputini Biodiversity Station (TBS) in Amazonian Ecuador. Our sample included 4 years of data on births (N = 36) and copulations (N = 170) for Lagothrix, 10 years of data on births (N = 35) and copulations (N = 74) for Ateles, and 7 years of data on ripe fruit availability. Reproductive events were distinctly seasonal. For both species, births were concentrated between May and September, a time period in which ripe fruit was relatively scarce, while inferred conceptions occurred between September and January, when ripe fruit availability was increasing and maintained at high‐levels throughout the forest. Interannual variation in births was relatively stable, except for in 2016 when twice as many infants were born following a strong El Niño event that may have led to unusually high levels of fruit productivity during the 2015 breeding season. Although copulations were observed year‐round, an overwhelming majority (>90% for Lagothrix and >80% for Ateles) took place between August and February when females were most likely to conceive. Collectively, these data follow the reproductive patterns observed in other atelin primates, and, as proposed by others, suggest that atelins may follow a risk‐averse breeding strategy.
Highlights
Both spider monkeys and woolly monkeys display reproductive seasonality in the patterns of copulations, conceptions, and births.
While births are more common during periods of low fruit availability, spider monkeys and woolly monkeys copulate and conceive at higher frequencies when fruit availability is increasing or maintained at high levels.
Consistent with capital breeding, both species had low infant mortality; interannual variation in births was influenced by fruit availability; and early months of gestation coincided with fruit abundance peaks, when females could store energy reserves.
Female mammals employ reproductive strategies (e.g., internal gestation) that result in power asymmetries specific to intersexual dyads. Because the number of eggs available for fertilization at any ...given time for most mammals is quite limited, having a fertilizable egg is potentially an important source of economic power for females. Control over mating opportunities is a source of intersexual leverage for female Verreaux’s sifaka (
Propithecus verreauxi
). We examined economic factors thought to influence the value of mating opportunities, and, thus, the extent of female leverage: kinship and market effects. Using a longitudinal dataset of agonistic interactions collected during focal animal sampling of all adult individuals in 10 social groups from 2008 to 2019, we tested the effects of relatedness, female parity, reproductive season, and adult sex ratio (population and group) on (1) the direction of submissive signaling and (2) which sex won a contested resource. While 96% of the acts of submission were directed from males toward females, females only won a third of their conflicts with males. Thus, our study has implications for evolutionary explanations of female-biased power. If female power evolved due to their greater need for food and other resources, then intersexual conflicts would be expected to result in males more consistently relinquishing control of resources. As expected, males were more likely to chatter submissively toward successful mothers, during the mating season, and when the sex ratio was male-biased. Although females generally had less power to win a conflict when their fertilizable egg was less valuable (when they were nulliparous or unsuccessful mothers or when interacting with male kin) and with an increasing female-bias in the sex ratio, this ability to win additionally was influenced by which sex initiated the conflict. Our study demonstrates that female leverage can be influenced by the supply and demand for mating opportunities, but evoking submission does not translate into winning a resource. Indeed, intersexual power is dynamic, contextual, and dependent on the individuals in the dyad.
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•We review major recent advances in Neotropical primate biogeography.•Evidence points to an Amazonian origin and long-term tropical habitation for Platyrrhini.•Intermittent Miocene ...connections led to Atlantic Forest colonizations from the Amazon.•Extant primate occupation of drier open ecoregions is due to recent expansions from rainforest.
New research presented in this special issue of Molecular Phylogenetics and Evolution on the “Phylogeny and Biogeography of Neotropical Primates” greatly improves our understanding of the evolutionary history of the New World monkeys and provides insights into the multiple platyrrhine radiations, diversifications, extinctions, and recolonizations that have taken place over time and over space in the Neotropics. Here, we synthesize genetic and biogeographic research from the past several years to construct an overarching hypothesis for platyrrhine evolution. We also highlight continuing controversies in Neotropical primate biogeography, such as whether the location of origin of platyrrhines was Africa or Asia; whether Patagonian fossil primates are stem or crown platyrrhines; and whether cis- and trans-Andean Neotropical primates were subject to vicariance through Andes mountain building, or instead diversified through isolation in mountain valleys after skirting around the Andes on the northwestern coast of South America. We also consider the role of the Amazon River and its major tributaries in shaping platyrrhine biodiversity, and how and when primates from the Amazon reached the Atlantic Forest. A key focus is on primate colonizations and extirpations in Central America, the Andes, and the seasonally dry tropical forests and savannas (such as the Llanos, Caatinga, and Cerrado habitats), all ecosystems that have been understudied up until now for primates. We suggest that most primates currently inhabiting drier open habitats are relatively recent arrivals, having expanded from rainforest habitats in the Pleistocene. We point to the Pitheciidae as the taxonomic group most in need of further phylogenetic and biogeographic research. Additionally, genomic studies on the Platyrrhini are deeply needed and are expected to bring new surprises and insights to the field of Neotropical primate biogeography.
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•Lagothrix lagothricha subspecies are not reciprocally monophyletic.•There are significantly different evolutionary units in Lagothrix lagothricha.•Different evolutionary units in ...Lagothrix lagothricha do not correlate with coat color.
The taxonomic history of the genus Lagothrix is complex, with molecular and morphological assessments giving conflicting results for the separation between its taxa. Phylogeographic studies of the most widely distributed species, Lagothrix lagotricha, have only been attempted recently and are limited to few individuals per collection site, many of which were captive making their geographical origin dubious. There is debate regarding the possibility of raising subspecies of Lagothrix lagotricha to the species level, therefore the geographical origin of samples is particularly relevant. In the present work we revisit the intraspecific phylogeography of L. lagotricha from northwestern South America, including the subspecies L. l. poeppiggi, L. l. lagotricha and L. l. lugens (sensu Fooden, 1963), using DNA sequence data from hypervariable region I of the mitochondrial control region (D-loop HVI). Our results suggest a complex picture in which there are well delimited evolutionary units that, nonetheless, do not correlate well with the morphological variation used to support the current delimitation of taxa. Additionally, we corroborate previous results showing a lack of reciprocal monophyly between the putative subspecies of Lagothrix lagotricha, and we propose that this may be due to ancestral polymorphism that has been maintained following the recent spread of woolly monkeys throughout the western Amazonian lowlands and into the inter-Andean region of Colombia.
Saki monkeys (Pithecia spp.) live in pairs and small groups, sometimes with more than 1 same-sex adult. Previous studies have not been able to distinguish additional, unrelated adults from ...adult-sized offspring, but both can influence social relationships and mating strategies, albeit in different ways. In this study, we documented the immigration of an adult male equatorial saki (P. aequatorialis) into a group following the departure of the previous resident male. At immigration, the group contained an adult female, her 5-year-old (adult age) and 1.5-year-old daughters, and her 1-month-old infant. We used nearest neighbor, approach, grooming, playing, aggression, and copulation data to describe the social dynamics between the immigrant male and the 2 adult females. In the 12 months following his arrival, the immigrant male tended to be closer to and groom the adult daughter more than the mother, but he mated with both females. Both females interacted more with the immigrant male than with each other, and both females eventually reproduced. These observations provide evidence that in equatorial sakis, adult offspring may delay dispersal and reproduce within their natal group, thus transitioning from groups of reproductive pairs to groups with more than 1 reproductive adult of the same sex.
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.
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