Intergroup encounters in pair-living primates: Comparative analysis and a case study of pair-living and monogamous owl monkeys (Aotus azarae) of Argentina.

The function of intergroup encounters (IGEs) may differ substantially among species of different group sizes and social organizations. Research in group-living primates has shown that the behavioral responses during IGEs can vary widely from affiliative to neutral or aggressive interactions; still, little is known about IGEs in pair-living taxa. We conducted a systematic literature review to find relevant studies on the functions of IGEs in pair-living nonhuman primates that could inform analyses of IGE data (n = 242 IGEs, 21 groups and 10 solitary individuals, 1997-2020) from wild owl monkeys, a pair-living, monogamous primate with extensive biparental care. We identified 1315 studies published between 1965 and 2021; only 13 of them (n = 10 species) contained raw data on the number of IGEs. Our review of those studies showed that IGEs are common, but highly variable in their nature and characteristics in pair-living primates. To examine the non-mutually exclusive hypotheses of resource-, and mate defense, and infanticide avoidance we analyzed data from the Owl Monkey Project 27-year long database to build first an a priori model set. To incorporate prior knowledge from the literature review, we conducted our analyses as a consecutive series of binomial logistic regressions. All IGEs including all biologically relevant parameters (N = 156) were codified into three different behavioral categories (Reaction, Agonism, and Physical Aggression). The analysis showed that owl monkeys regularly engaged in IGEs, most of which were agonistic. They showed more reaction when infants were present, but reactions were less physically aggressive when infants and pregnant females were involved. Overall, our results lend more support for the infant and mate defense hypotheses than they do for the resource defense one.

Associations between fecal cortisol and biparental care in a pair-living primate.

OBJECTIVES: We quantified variation in fecal cortisol across reproductive periods in Azara's owl monkeys (Aotus azarae) to examine physiological mechanisms that may facilitate biparental care. Specifically, we evaluated evidence for the explanation that owl monkeys have hormonal mechanisms to mobilize energy during periods when each sex is investing heavily in reproduction, that is, the gestation period for females and the infant care period for males. MATERIALS AND METHODS: Between 2011 and 2015, we monitored 10 groups of Azara's owl monkeys from a wild population in Formosa, Argentina and collected fecal samples from 26 adults (13 males, 13 females). Using enzyme-linked immunosorbent assays, we quantified fecal cortisol as a proxy for evaluating stress responses, including energetic demands, on both sexes during periods of reproduction and parental care. RESULTS: Male cortisol was lowest during periods when they were caring for young infants (<3 months) compared with periods with older infants or no infant. Female cortisol was elevated during gestation compared with other periods. Mean fecal cortisol in both males and females was lower when an infant was present compared with when females were gestating. DISCUSSION: Our results do not support the hypothesis that owl monkey males have elevated fecal cortisol during periods when they need to mobilize energy to provide intensive infant care. Our findings are also inconsistent with the Maternal Relief hypothesis. However, results from studies measuring fecal cortisol must be interpreted with care and alternative explanations, such as seasonal fluctuations in diet and thermoenergic demands, should be considered when drawing conclusions.

Ranging behavior and the potential for territoriality in pair-living titi monkeys (Plecturocebus discolor).

Patterns of ranging behavior and space use are key for evaluating current ideas about the evolution and maintenance of pair-living and sexual monogamy as they provide insights into the dispersion of females, the potential for territoriality, and whether males are limited to defending an area that can support only one female and her offspring. We examined ranging behavior and space use to evaluate the potential for territoriality in five groups of red titi monkeys (Plecturocebus discolor) during a 10-year study in Ecuadorian Amazonia. Mean home range size, calculated using a time-sensitive local convex hull estimation procedure, was 4.0 ± 1.4 ha. Annual home ranges of neighboring groups overlapped, on average, 0%-7%. Mean daily path length was 670 ± 194 m, resulting in defendability indices of 2.2-3.6 across groups. Groups visited, on average, 4 of 12 sections of their home range border area per day, but that was not more often than would be expected by chance, and intergroup encounters were infrequent. We did not find evidence of active monitoring for intruders in border areas, in that groups did not travel either faster or slower when at the border than when in central areas of their range. The absence of overt monitoring might be compensated for by engaging in loud calls, which the study groups did throughout their home ranges; these calls may serve as an advertisement of occupancy and a deterrent to intruding conspecifics. Our finding that red titis have a high potential for territoriality is consistent with several of the main hypotheses proposed to explain pair-living in mammals.

Access to electric light is associated with delays of the dim-light melatonin onset in a traditionally hunter-gatherer Toba/Qom community.

Key to the transition of humans from nomadic hunting-gathering groups to industrialized and highly urbanized societies was the creation of protected and artificially lit environments that extended the natural daylight hours and consolidated sleep away from nocturnal threats. These conditions isolated humans from the natural regulators of sleep and exposed them to higher levels of light during the evening, which are associated with a later sleep onset. Here, we investigated the extent to which this delayed timing of sleep is due to a delayed circadian system. We studied two communities of Toba/Qom in the northern region of Argentina, one with and the other without access to electricity. These communities have recently transitioned from a hunting-gathering subsistence to mixed subsistence systems and represent a unique model in which to study the potential effects of the access to artificial light on sleep physiology. We have previously shown that participants in the community with access to electricity had, compared to participants in the community without electricity, later sleep onsets, and shorter sleep bouts. Here, we show they also have a delayed dim-light melatonin onset (DLMO). This difference is present during the winter but not during the spring when the influence of evening artificial light is likely less relevant. Our results support the notion that the human transition into artificially lit environments had a major impact on physiological systems that regulate sleep timing, including the phase of the master circadian clock.

The evolution of pair-living, sexual monogamy, and cooperative infant care: Insights from research on wild owl monkeys, titis, sakis, and tamarins.

"Monogamy" and pair bonding have long been of interest to anthropologists and primatologists. Their study contributes to our knowledge of human evolutionary biology and social evolution without the cultural trappings associated with studying human societies directly. Here, we first provide an overview of theoretical considerations, followed by an evaluation of recent comparative studies of the evolution of "social monogamy"; we are left with serious doubts about the conclusions of these studies that stem from the often poor quality of the data used and an overreliance on secondary sources without vetting the data therein. We then describe our field research program on four "monogamous" platyrrhines (owl monkeys, titis, sakis, and tamarins), evaluate how well our data support various hypotheses proposed to explain "monogamy," and compare our data to those reported on the same genera in comparative studies. Overall, we found a distressing lack of agreement between the data used in comparative studies and data from the literature for the taxa that we work with. In the final section, we propose areas of research that deserve more attention. We stress the need for more high-quality natural history data, and we urge researchers to be cautious about the uncritical use of variables of uncertain internal validity. Overall, it is imperative that biological anthropologists establish and follow clear criteria for comparing and combining results from published studies and that researchers, reviewers, and editors alike comply with these standards to improve the transparency, reproducibility, and interpretability of causal inferences made in comparative studies.

The diversity of population responses to environmental change.

The current extinction and climate change crises pressure us to predict population dynamics with ever-greater accuracy. Although predictions rest on the well-advanced theory of age-structured populations, two key issues remain poorly explored. Specifically, how the age-dependency in demographic rates and the year-to-year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age-specific demographic rates and when ages are reduced to stages. We find that stage- vs. age-based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival-fecundity-trade-offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age-specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.

Testing the weekend effect hypothesis: Time of day and lunar phase better predict the timing of births in laboratory-housed primates than day of week.

The weekend effect hypothesis proposes that captive primates are more likely to give birth during times of low disturbance and reduced staff activity. The hypothesis specifically predicts that laboratory-housed primates will be more likely to give birth during the weekend than weekdays when staff activity is reduced. To date, support for the weekend effect hypothesis has been mixed and based on studies with relatively few subjects. To further examine the hypothesis, we analyzed the birthing patterns of three genera of laboratory-housed primates: squirrel monkeys (Saimiri species, N = 2,090 births), owl monkeys (Aotus species, N = 479 births), and rhesus macaques (Macaca mulatta, N = 2,047 births). Contrary to predictions derived from the weekend effect hypothesis, the frequencies of births during weekends for all taxa were not significantly different from rates that would be expected by chance. However, while there was no variance across days of the week, all three taxa gave birth at nighttime, when staff was absent. This parallels reports of births in wild and captive monkeys, both diurnal and nocturnal, which are more likely to give birth during the night; plausibly a time when the environmental and social disturbance is lowest and the mother is safest to bond with her newborn infant. As all births occurred at night, we also explored the relationship between the lunar cycle and the timing of births timing. While the diurnal primates (i.e., Saimiri and Macaca) were no more likely to give birth on "bright" nights than "dark" nights, owl monkeys (Aotus) had a much higher frequency of births on bright nights than darker ones, and at rates that deviated from chance. Our data provide a more detailed understanding on how the environment may influence captive monkey births but do not support the oft-cited weekend effect hypothesis.

Ranging behavior and potential for territoriality in equatorial sakis (Pithecia aequatorialis) in Amazonian Ecuador.

OBJECTIVES: Territoriality refers to the consistent defense of an area within the home range (HR) against intrusions of conspecifics. It implies exclusive space use with low degree of overlap among neighboring groups, high site fidelity, specific ranging behavior such as high mobility relative to HR size and frequent visits of territory borders, and monitoring behavior. We examined ranging behavior and use of space to evaluate territoriality in Pithecia aequatorialis in Ecuador. MATERIALS AND METHODS: Between 2005 and 2015, we monitored one main study group continuously and five additional groups for shorter periods (5 months to 2.5 years) at the Tiputini Biodiversity Station, in eastern Ecuador. We scored the location of the study groups at 20 min intervals during, on average, 5 days per month. We estimated saki HRs and core areas (CAs) using the fixed kernel density method (95 and 50%, respectively). RESULTS: The average HR size was 57 ha and the average CA 14 ha. The degree of overlap between HRs of neighboring groups was low (2-9%). For the main study group, the average overlap between annual HRs was 82%. Mean daily path length across groups was 1,151 m; the defensibility index varied between 1.1 and 2.3 (values >1 are suggestive of territoriality), and the fractional monitoring rate varied between 0.06 and 0.15 (values >0.08 are suggestive of territoriality). Groups did not visit their HR borders (100 m inner buffer) more often than would be expected by chance. Travel speed and directness were comparable between the borders and the centers of groups' HRs. DISCUSSION: Our multiyear study suggests that equatorial sakis show low degree of range overlap and high site fidelity and have the potential to be territorial, given their high mobility relative to HR size that allows for frequent border monitoring. Nevertheless, their movement patterns in border areas did not reveal evidence for monitoring behavior.

Are olfactory traits in a pair-bonded primate under sexual selection? An evaluation of sexual dimorphism in Aotus nancymaae.

OBJECTIVES: Sexual selection has seemingly influenced chemical communication in numerous non-human primates, although it is unclear whether it has influenced strictly pair-living and pair-bonded taxa. The physical similarities between male and female owl monkeys suggest that disruptive selection has not played a role in this taxon. However, given their nocturnality, olfactory traits may show differing patterns of sexual selection than visual traits. If sexual selection has influenced chemical communication in owl monkeys, we expect larger scent glands and greater scent-marking in females given the high degree of paternal care, as has been proposed for callitrichines. MATERIALS AND METHODS: We evaluated sex differences in the qualitative and quantitative descriptions of the subcaudal and perianal glandular regions of captive male (n = 39) and female (n = 36) owl monkeys (A. nancymaae), and in the olfactory behaviors performed within breeding pairs (n = 16). RESULTS: Males had larger areas of secretion retained in the hairs covering the subcaudal gland, and females had more and darker secretion than males covering the perianal region. Males inspected the genital region of their partners more frequently than females did, but the sexes did not differ much in other investigative and marking behaviors. DISCUSSION: The observed sex differences and variation in olfactory traits are consistent with the hypothesis that sexual selection has influenced chemical communication in owl monkeys, with males having larger subcaudal glands and spending more time investigating odors. Still, sex differences in monogamous owl monkeys were less extreme than those in other, non-monogamous, taxa.

Chemical composition of glandular secretions from a pair-living monogamous primate: Sex, age, and gland differences in captive and wild owl monkeys (Aotus spp.).

Broadening our knowledge of olfactory communication in strictly monogamous systems can inform our understanding of how chemosignals may facilitate social and reproductive behavior between the sexes. Compared to other social and mating systems, relatively little is known about olfactory communication in strictly monogamous non-human primates. Furthermore, platyrrhines are not well represented in chemical analyses of glandular secretions. We conducted semi-quantitative headspace gas chromatography with mass spectrometry to investigate the chemical components of glandular secretions from the subcaudal and pectoral glands of a strictly pair-living platyrrhine, the owl monkey (Aotus spp.). In this study, the first chemical analysis of a wild platyrrhine population, our goals were to (1) conduct a robust analysis of glandular secretions from both captive and wild owl monkey populations and (2) identify whether biologically relevant traits are present in glandular secretions. We also compared and contrasted the results between two Aotus species in different environmental contexts: wild Aotus azarae (N = 33) and captive A. nancymaae (N = 104). Our findings indicate that secretions from both populations encode sex, gland of origin, and possibly individual identity. These consistent patterns across species and contexts suggest that secretions may function as chemosignals. Our data also show that wild A. azarae individuals are chemically discriminated by age (adult or subadult). Among the captive A. nanycmaae, we found chemical differences associated with location, possibly caused by dietary differences. However, there was no noticeable effect of contraception on the chemical profiles of females, nor evidence that closely related individuals exhibit more similar chemical profiles in A. nancymaae. Overall, our data suggest that glandular secretions of both wild and captive Aotus convey specific information. Future studies should use behavioral bioassays to evaluate the ability of owl monkeys to detect signals, and consider whether odor may ultimately facilitate social and sexual relationships between male and female owl monkeys.

Hormonal correlates of development and natal dispersal in wild female owl monkeys (Aotus azarae) of Argentina.

Pair-living and socially monogamous primates typically do not reproduce before dispersing. It is currently unclear whether this reproductive suppression is due to endocrine or behavioral mechanisms. Cooperatively breeding taxa, like callitrichids, may forego reproduction in natal groups because they reap inclusive fitness benefits and/or they are avoiding inbreeding. However, neither of these benefits of delayed reproduction appear to adequately explain the lack of reproduction prior to leaving the natal group in pair-living monogamous species. In this study, we determined whether wild Azara's owl monkeys (Aotus azarae) in the Argentinean Chaco establish reproductive maturity prior to dispersing. We utilized 635 fecal extracts to characterize reproductive hormone profiles of 11 wild juvenile and subadult females using enzyme immunoassays. Subadult females showed hormone profiles indicative of ovulatory cycling and had mean PdG and E1G concentrations approximately five times higher than juveniles. Contrary to expectations from the inbreeding avoidance hypothesis, female owl monkeys do not delay puberty, but rather commence ovarian cycling while residing in their natal group. Still, subadults appear to have a period during which they experience irregular, non-conceptive cycles prior to reproducing. Commencing these irregular cycles in the natal group may allow them to develop a state of suspended readiness, which could be essential to securing a mate, while avoiding costs of ranging solitarily. Our results indicate that reproductive suppression in female owl monkeys is not due to endocrine suppression. We suggest that adults likely use behavioral mechanisms to prevent subadults from reproducing with unrelated adult males in their natal group.

The role of intragroup agonism in parent-offspring relationships and natal dispersal in monogamous owl monkeys (Aotus azarae) of Argentina.

Agonistic behaviors are common in many group-living taxa and may serve a variety of functions, ranging from regulating conflicts over reproduction to defending food resources. However, high rates of agonism are not expected to occur among close relatives or individuals in established mating relationships, which are characteristics of monogamous groups. To contribute to our understanding of agonism within socially monogamous groups, we collected behavioral and demographic data from Azara's owl monkeys (Aotus azarae) in the Gran Chaco of Argentina over 14 years. We examined factors related to age, sex, kinship, and behavioral context to evaluate predictions of the hypotheses that agonism functions to regulate dispersal and that it mediates competition for food and/or mates. Intragroup agonism was relatively rare: the group rate was approximately one event every three and a half hours. Rates of agonism were generally similar for both sexes, but there were marked differences among age categories. Agonism performed by adults was more frequently directed at subadults than at younger offspring. In contrast, agonistic interactions involving infants were very rare. Among interactions between adults and subadults, adults were much more frequently the actors than the recipients, suggesting that agonism from adults may influence natal dispersal of subadults. Agonistic events were most frequent during foraging, but also occurred more frequently than expected during bouts of social behavior. Overall, our results suggest that agonism in owl monkeys serves as a mechanism for regulating dispersal, and also likely plays a role in mediating mating and feeding competition.

Delayed Dispersal and Immigration in Equatorial Sakis (Pithecia aequatorialis): Factors in the Transition from Pair- to Group-Living.

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.

Transparency, usability, and reproducibility: Guiding principles for improving comparative databases using primates as examples.

Recent decades have seen rapid development of new analytical methods to investigate patterns of interspecific variation. Yet these cutting-edge statistical analyses often rely on data of questionable origin, varying accuracy, and weak comparability, which seem to have reduced the reproducibility of studies. It is time to improve the transparency of comparative data while also making these improved data more widely available. We, the authors, met to discuss how transparency, usability, and reproducibility of comparative data can best be achieved. We propose four guiding principles: 1) data identification with explicit operational definitions and complete descriptions of methods; 2) inclusion of metadata that capture key characteristics of the data, such as sample size, geographic coordinates, and nutrient availability (for example, captive versus wild animals); 3) documentation of the original reference for each datum; and 4) facilitation of effective interactions with the data via user friendly and transparent interfaces. We urge reviewers, editors, publishers, database developers and users, funding agencies, researchers publishing their primary data, and those performing comparative analyses to embrace these standards to increase the transparency, usability, and reproducibility of comparative studies.

Social monogamy in wild owl monkeys (Aotus azarae) of Argentina: the potential influences of resource distribution and ranging patterns.

Using published and new data from a population of monogamous owl monkeys in the Argentinean Chaco, I examine the hypothesis that social monogamy is a default social system imposed upon males because the spatial and/or temporal distribution of resources and females makes it difficult for a single male to defend access to more than one mate. First, I examine a set of predictions on ranging patterns, use of space, and population density. This first section is followed by a second one considering predictions related to the abundance and distribution of food. Finally, I conclude with a section attempting to link the ranging and ecological data to demographic and life-history parameters as proxies for reproductive success. In support of the hypothesis, owl monkey species do live at densities (7-64 ind/km(2) ) that are predicted for monogamous species, but groups occupy home ranges and core areas that vary substantially in size, with pronounced overlap of home ranges, but not of core areas. There are strong indications that the availability of food sources in the core areas during the dry season may be of substantial importance for regulating social monogamy in owl monkeys. Finally, none of the proxies for the success of groups were strongly related to the size of the home range or core area. The results I present do not support conclusively any single explanation for the evolution of social monogamy in owl monkeys, but they help us to better understand how it may function. Moreover, the absence of conclusive answers linking ranging, ecology, and reproductive success with the evolution of social monogamy in primates, offer renewed motivation for continuing to explore the evolution of monogamy in owl monkeys.

Demography and life history of wild red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia aequatorialis) in Amazonian Ecuador: A 12-year study.

We investigated demographic patterns and life history traits from several groups of red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia aequatorialis) monitored throughout the first 12 years (November 2003 through May 2015) of an ongoing research project in the Yasuní National Park and Biosphere Reserve, Ecuador. The saki groups ranged in size between two and six individuals, comprising either one adult male and one adult female or multiple adult-sized males or females, plus immatures. Deviations from a pair-living structure resulted when two different daughters of the resident female grew up and successfully reproduced in their natal group and when an adult-sized male temporarily immigrated into the group when it already contained an adult male. The titi groups also ranged in size between two and six individuals, but almost exclusively lived in groups with one adult individual of each sex. No titi offspring were observed to breed in their natal groups, and both male and female offspring dispersed when they were between 2.1 and 5.0 years old. In both titi and saki groups, vacant breeding positions resulting from the disappearance of an adult group member were promptly occupied by immigrants of the same sex as the disappeared group member. We recorded nine saki and 28 titi births. Eighty-three percent of the titi births occurred between September and January, suggesting reproductive seasonality. The mean interbirth interval after an infant survived its first 6 months was 21.3 ± SE 1.9 months (N = 3) for sakis and 14.5 ± SE 1.5 months (N = 14) for titis. Saki infant survival was 70%, and juvenile survival 57%. Titi infant survival was 88%, and juvenile survival was 53%. This 12-year study provides important insights into the functioning and maintenance of pair-living and social monogamy in two little-known platyrrhine species.

Age and sex-specific mortality of wild and captive populations of a monogamous pair-bonded primate (Aotus azarae).

In polygynous primates, a greater reproductive variance in males have been linked to their reduced life expectancy relative to females. The mortality patterns of monogamous pair-bonded primates, however, are less clear. We analyzed the sex differences in mortality within wild (NMales = 70, NFemales = 73) and captive (NMales = 25, NFemales = 29) populations of Azara's owl monkeys (Aotus azarae), a socially and genetically monogamous primate exhibiting biparental care. We used Bayesian Survival Trajectory Analysis (BaSTA) to test age-dependent models of mortality. The wild and captive populations were best fit by the logistic and Gompertz models, respectively, implying greater heterogeneity in the wild environment likely due to harsher conditions. We found that age patterns of mortality were similar between the sexes in both populations. We calculated life expectancy and disparity, the latter a measure of the steepness of senescence, for both sexes in each population. Males and females had similar life expectancies in both populations; the wild population overall having a shorter life expectancy than the captive one. Furthermore, captive females had a reduced life disparity relative to captive males and to both sexes in the wild. We interpret this pattern in light of the hazards associated with reproduction. In captivity, where reproduction is intensely managed, the risks associated with gestation and birth are tempered so that there is a reduction in the likelihood of captive females dying prematurely, decreasing their overall life disparity.

Oxytocin receptor gene sequences in owl monkeys and other primates show remarkable interspecific regulatory and protein coding variation.

The oxytocin (OT) hormone pathway is involved in numerous physiological processes, and one of its receptor genes (OXTR) has been implicated in pair bonding behavior in mammalian lineages. This observation is important for understanding social monogamy in primates, which occurs in only a small subset of taxa, including Azara's owl monkey (Aotus azarae). To examine the potential relationship between social monogamy and OXTR variation, we sequenced its 5' regulatory (4936bp) and coding (1167bp) regions in 25 owl monkeys from the Argentinean Gran Chaco, and examined OXTR sequences from 1092 humans from the 1000 Genomes Project. We also assessed interspecific variation of OXTR in 25 primate and rodent species that represent a set of phylogenetically and behaviorally disparate taxa. Our analysis revealed substantial variation in the putative 5' regulatory region of OXTR, with marked structural differences across primate taxa, particularly for humans and chimpanzees, which exhibited unique patterns of large motifs of dinucleotide A+T repeats upstream of the OXTR 5' UTR. In addition, we observed a large number of amino acid substitutions in the OXTR CDS region among New World primate taxa that distinguish them from Old World primates. Furthermore, primate taxa traditionally defined as socially monogamous (e.g., gibbons, owl monkeys, titi monkeys, and saki monkeys) all exhibited different amino acid motifs for their respective OXTR protein coding sequences. These findings support the notion that monogamy has evolved independently in Old World and New World primates, and that it has done so through different molecular mechanisms, not exclusively through the oxytocin pathway.

A Saki Saga: Dynamic and Disruptive Relationships among Pithecia aequatorialis in Ecuador.

Saki monkeys live in socially monogamous groups and in groups containing more than one same-sex adult. As part of a 10-year study of equatorial sakis (Pithecia aequatorialis) in Ecuador, we documented the immigration of a second adult male into a group containing a resident male-female pair that had associated with one another for seven years and the resident female's two daughters. In the first month after immigration, the resident male spent more time closer to and grooming his putative adult daughter than the resident female, and the two males were seen performing a cooperative territorial display. After two months, the resident male interacted more with the resident female than with his putative adult daughter, while that daughter interacted more with the immigrant male and copulated with him. After three months, the males left the group together and associated with an unfamiliar female, leaving the resident females and a neonate behind. The resident male then paired with a new female, while the immigrant male joined another group, again as a second male. Compared to other socially monogamous primates, sakis appear to have a more variable social system whereby additional males can join established groups and form relationships with putatively unrelated males.

Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys.

Understanding the evolution of mating systems, a central topic in evolutionary biology for more than 50 years, requires examining the genetic consequences of mating and the relationships between social systems and mating systems. Among pair-living mammals, where genetic monogamy is extremely rare, the extent of extra-group paternity rates has been associated with male participation in infant care, strength of the pair bond and length of the breeding season. This study evaluated the relationship between two of those factors and the genetic mating system of socially monogamous mammals, testing predictions that male care and strength of pair bond would be negatively correlated with rates of extra-pair paternity (EPP). Autosomal microsatellite analyses provide evidence for genetic monogamy in a pair-living primate with bi-parental care, the Azara's owl monkey (Aotus azarae). A phylogenetically corrected generalized least square analysis was used to relate male care and strength of the pair bond to their genetic mating system (i.e. proportions of EPP) in 15 socially monogamous mammalian species. The intensity of male care was correlated with EPP rates in mammals, while strength of pair bond failed to reach statistical significance. Our analyses show that, once social monogamy has evolved, paternal care, and potentially also close bonds, may facilitate the evolution of genetic monogamy.