Inbreeding avoidance, competition and natal dispersal in a pair-living, genetically monogamous mammal, Azara's owl monkey (Aotus azarae)

Abstract

Natal dispersal is an important life-history stage influencing individual fitness, social dynamics of groups and population structure. Understanding factors influencing dispersal is essential for evaluating explanations for the evolution and maintenance of social organization, including parental care and mating systems. The social and mating systems of Azara's owl monkeys (Aotus azarae) are infrequent among mammals; these primates are pair-living, serially and genetically monogamous and both sexes directly care for offspring. To evaluate the role that competition and inbreeding avoidance play in shaping dispersal patterns, we used 25 years of demographic and genetic data to examine how variation in timing of natal dispersal is related to social (adult replacements, step-parents, births and group size) and ecological factors (seasonal abundance of resources) in a wild population of A. azarae in Formosa, Argentina. We found that all males and females dispersed from their natal groups, but subadults delayed dispersal when a step-parent of the opposite sex joined the group, indicating that they may perceive these step-parents as potential mates. Dispersal was more probable when resource conditions were better, regardless of age. Overall, agonistic conflict over food and potential mates with adults in the natal group, as well as inbreeding avoidance, contribute to regulating dispersal.

Headnote

Keywords:

dispersal, inbreeding avoidance, competition, owl monkey

Natal dispersal is an important life-history stage influencing individual fitness, social dynamics of groups and population structure. Understanding factors influencing dispersal is essential for evaluating explanations for the evolution and maintenance of social organization, including parental care and mating systems. The social and mating systems of Azara's owl monkeys (Aotus azarae) are infrequent among mammals; these primates are pair-living, serially and genetically monogamous and both sexes directly care for offspring. To evaluate the role that competition and inbreeding avoidance play in shaping dispersal patterns, we used 25 years of demographic and genetic data to examine how variation in timing of natal dispersal is related to social (adult replacements, step-parents, births and group size) and ecological factors (seasonal abundance of resources) in a wild population of A. azarae in Formosa, Argentina. We found that all males and females dispersed from their natal groups, but subadults delayed dispersal when a step-parent of the opposite sex joined the group, indicating that they may perceive these step-parents as potential mates. Dispersal was more probable when resource conditions were better, regardless of age. Overall, agonistic conflict over food and potential mates with adults in the natal group, as well as inbreeding avoidance, contribute to regulating dispersal.

1. Introduction

Natal dispersal (hereafter dispersal), the movement of individuals from their birthplace to areas in which they may breed, is a critical process that influences the fitness of individuals, group demogra-phy, social dynamics and the genetic structure of groups and populations [1,2]. From the perspective of an individual, dispersal is a behavioural strategy that has major consequences for the individual's health and survival [3]. Dispersal has profound impacts on social organisms, in particular, as it affects the availability of potential social and mating partners. It thus influences access to reproductive opportunities, and ultimately helps to determine an individual's fitness [4-6]. At the level of the group, whether individuals disperse or remain in the natal group to breed impacts social dynamics within and between groups, patterns of relatedness and the potential for indirect fitness [7,8]. At the level of the population, patterns of dispersal impact gene flow and community dynamics [1,9,10], ultimately shaping patterns of biodiversity [2]. Documenting the individual, group and population implications of dispersal is essential for explaining the evolution of social and mating systems [11-14], and for effectively managing populations and predicting the consequences that environmental changes may have on species' distributions [15-17].

The study of dispersal had an initial historical focus on examining the relationships between mating systems and life-history traits to explain variation in patterns of dispersal [11,13,18-20], later enriched with attention to the evolutionary history of the taxa [21-23]. In the last several decades, the 'genetics' revolution generated a new set of theoretical and empirical evidence showing that the relationship between dispersal patterns and mating systems is more complex than had traditionally been assumed [2,14,24-26]. These advances led to a variety of new theoretical explanatory models, that look beyond phylogeny or mating systems, to provide adaptive explanations for why, when and how individuals leave their natal groups [27-29].

Over all these years, two main hypotheses have guided the research on the evolution of dispersal. The inbreeding avoidance hypothesis states that the evolution of dispersal is driven by the risks of mating with close kin if staying in the natal group [11,13,20,23,30-32]. Inbreeding avoidance is the hypothesis most often invoked for explaining dispersal in pair-living taxa [13,23,32]. In these species, offspring of both sexes lack access to unrelated potential mates and must therefore disperse in order to avoid breeding with close kin. However, animals may not always avoid inbreeding [33,34] and serial monogamy and extra-pair mating can lead to situations in which individuals who have yet to disperse can gain access to unrelated opposite-sex adults [35,36]. The competition avoidance hypothesis states that the evolution of dispersal is primarily driven by a need to minimize the fitness detriments of competing with kin for access to mates or resources [11,13,29]. Based on this hypothesis, factors such as group size, the introduction of new (unrelated) individuals to the group, local population density and food availability in the natal territory may influence the relative amount of competition for resources with kin and thus the likelihood of dispersal [37-42].

Evaluating explanations for complex behaviours, such as dispersal, is challenging, especially in wild populations of relatively long-lived taxa. Diverse influences, including individual (e.g. sex, size and body condition), social (e.g. natal group composition, density of mates and/or competitors) and ecological (availability of food, territories, etc.) factors, may all contribute to dispersal decisions [3,29,39]. It is therefore necessary to understand the behavioural ecology, social and mating system of a species, including information on tenure length, patterns of parental care and relatedness within groups [30,43]. Knowing the genetic structure of groups is essential for explaining why individuals of one sex, or both sexes, leave their natal groups; thus, genetic data can provide important insights into general patterns of dispersal and gene flow. However, to determine how social and ecological factors influence dispersal requires multi-year demographic monitoring of identified groups of individuals. Combining demographic information with genetic data on identity and parentage is a powerful means of assessing how relatedness and familiarity influence dispersal decisions, and the effects that dispersal has on individuals, groups and populations.

Here, we leverage demographic, life-history and genetic data to evaluate how well the resource competition and inbreeding avoidance hypotheses explain dispersal patterns in owl monkeys. Dispersal is a multi-phase life-history process that can include emigration (leaving from the natal area), a transient phase (i.e. floating [44]) and immigration (settling in a new area) [9,45], and each of these phases may be under specific selective forces to reduce the overall cost of dispersal [3,25]. In this study, we focus on the first of these phases, the timing of emigration, and examine social and ecological factors that may influence when individuals leave their natal group.

The Azara's owl monkey (Aotus azarae azarae) is a pair-living, monogamous, arboreal primate that exhibits biparental care. The population of owl monkeys in Formosa, Argentina, is composed of social groups consisting of two reproducing adults, which are genetically monogamous [46], and 1-4 young [47]. The population also includes 4-9 solitary floater individuals per square kilometre [44]. Both adult males and adult females are replaced regularly by these floaters; the resulting serial monogamy means that young are frequently living in natal groups with unrelated adults who represent potential mates or mate competitors [48,49]. Analyses of demographic data offered some preliminary findings on dispersal patterns [50,51].

We present here analyses spanning 25 years, during which we monitored the composition and demographic changes of groups, ecological variables and collected biological samples, from which genetic marker data were obtained. We use these data to describe dispersal patterns and evaluate proximate factors that may be influencing variation in the age and timing of natal dispersal in this pair-living primate. We examine how social and ecological variables (i.e. group size, infant births, adult replacements and food availability) contribute to variation in the age and timing of natal dispersal. Specifically, we predict that if inbreeding avoidance is the primary cause of dispersal, then dispersals will consistently occur before, or around, the time individuals reach sexual maturity. Even when serial monogamy sometimes introduces unrelated step-parents to the natal group, these potential mates are not always available to the young; some pairs of reproducing adults maintain their relationship over a decade, indicating that inbreeding avoidance may still be important in this population. If resource competition is an important factor, dispersals will occur more frequently in particular seasons associated with different valuable resources (e.g. mating and food). Since dispersal is costly, owl monkeys will generally disperse during seasons (e.g. spring) when food resources are most abundant. However, offspring may be forced to disperse at less than ideal times of the year when conditions are particularly harsh, if food competition with natal group members becomes more intense. In this case, dispersals will occur during the harsh, winter months, at times when fruit abundance is lower. If mating competition is an important driver, then the timing of dispersals will be influenced by adult replacements that introduce potential mates/mate competitors to the natal group. We predict that the influence of an adult replacement will depend on the age and sex of the offspring, relative to the new adult. If the replacement occurs prior to the sexual maturity of the offspring, we do not predict it to consistently influence the mean age, or timing, of dispersal. However, if a replacement occurs after an offspring begins to undergo sexual maturity (e.g. a subadult), we predict two alternative outcomes: offspring in the presence of a potential mate remain in their natal group longer, in order to retain access to the new potential mate, or they leave the natal group sooner because they are expelled by their same-sexed genetic parent with whom they are now experiencing mate competition.

2. Methods

2.1. Study site

We studied the natal dispersal of Azara's owl monkeys (A. azarae azarae) at the Reserva Privada Mono Mirikiná, a 1500 ha reserve on a private cattle ranch in the Humid Chaco of Formosa, Argentina. The Owl Monkey Project (OMP) of Argentina has studied this owl monkey population at Estancia Guay colee (58°13' W, 25°54' S) since 1996 [52,53]. Specifically, a 300 ha area of gallery forest along the banks of the Riacho Pilagá has been mapped and groups within this area have been habituated. Owl monkeys (A. azarae) at this site live in both the gallery forest and forest patches; the data reported here come from groups residing in the gallery forest, with the exception of one group, Colman, which resides in a xerophytic forest patch next to the core study area. An additional description of the site and methods are provided in the electronic supplementary material.

2.2. Data collection

Demographic data: To identify changes in group composition (i.e. births, replacements, dispersals and deaths) we used a combination of regular monitoring of identified, habituated groups and information on genetic identity and parentage. Each time we contacted a group, the observer recorded the structure of the group (size and age of each group member) and the identity of each previously identified individual to document changes in group composition since the previous sighting. The unequivocal identification of individuals is facilitated by the presence of bead and radio collars [8,54]. We excluded individuals for which the dates of birth or dispersal could not be estimated with an accuracy of at least six months (i.e. the animal is first noticed as missing more than a year after it was last seen in the group).

Our dataset included 329 births in 29 groups recorded between September 1996 and December 2021 (table 1). Adult replacements were determined from changes in group composition as described above. Regarding 'dispersals', we classified the absence of an individual from its natal group between 1997 and 2020 in one of the three categories: presumed dispersal, confirmed dispersal or dead (table 1). A 'presumed dispersal' refers to an individual, 18 months or older, missing from its natal group that was not seen again outside of the natal group. We chose 18 months as the minimum age for a potential dispersal because this is the youngest age when an offspring in the study population has been confirmed to leave the natal group and survive independently. We use 'confirmed dispersal' for an individual that, after leaving its natal group, we observed ranging solitarily, or living as an adult in a new group. We distinguish between presumed and confirmed dispersal because, while it is reasonable to presume that a missing offspring >18 months has dispersed, it is still possible that some of them may be missing because they died while still in their natal groups. We classified an individual less than 18 months old as 'dead' when missing from its natal group; those 18 months or older were considered 'dead' when observers could identify the remains of a particular individual within the home range of the natal group.

Sampling: Biological material (i.e. ear punches, blood or hair) was collected from 173 unique individuals during captures; still, most samples used for DNA analyses presented here were obtained non-invasively by recovering faeces from the forest floor immediately after an identified animal defecated (n = 602 faecal samples). We used these samples to determine the genetic sex of dispersing individuals [55] and to establish genetic relationships among group members using microsatellite genotypes.

Microsatellite data collection: To assess identity and parentage we developed a panel of 22 microsa-tellite loci by screening the genome for A. azarae made available to us in advance by J. Rogers and colleagues [56]. From this screening, we identified 50 potential variable loci, all from different contigs, for which sequences with M-13 tails on forward primers were designed [57]. Primers for these 50 candidate loci were tested with a subset of 20 DNA extracts from owl monkeys sampled in Formosa, Argentina. We selected 22 loci that amplified consistently and showed variation in the study population for subsequent analyses used to identify individuals and parentage (electronic supplementary material, table SI). Microsatellite genotypes were used to establish identities of uncaptured individuals and establish genetic relationships among group members (i.e. to determine if pre-dispersing young were living with genetic parents or with one or more unrelated step-parents).

Ecological data: There is a strong seasonal pattern in the forest's productivity, with the availability of owl monkey food sources reaching a nadir during the winter dry season (June-August). For analyses of the relationship between resource competition and dispersal, we used counts of fruit from the four most important dry season fruit-producing species, to create an index of winter fruit availability for each year in each owl monkey group's home range. Specifically, we used phenological data, collected monthly from approximately 300 trees in plots located in the core of the OMP's study area from 2003 to 2021 [58,59] (see electronic supplementary material for details).

2.3. Data analysis

We calculated summary statistics for the age at dispersal and the time to dispersal after an adult replacement. We also constructed 'survival curves' to show the proportion of individuals remaining in the natal group at a given age for confirmed and presumed dispersals (electronic supplementary material, figure SI), for male and female dispersers (figure 1), and for the time to dispersal for subadults that experienced adult replacements (figure 2). We summarized the seasonality of dispersal by calculating the proportion of dispersals that occurred in each month and in each season (electronic supplementary material, figure S4).

When modelling our data, we conducted three sets of analyses. Set 1 examines the relationship between social composition of the natal group and age at dispersal. Set 2 investigates the relationship between adult replacements and time to dispersal. Set 3 explores the relationships between social and ecological factors and the seasonality of dispersal. For each of the three, we took an information theoretic approach [60,61] and defined an a priori set of models (Cox regression models for Sets 1 and 2; generalized linear regression models for Set 3). We chose explanatory variables (table 2) for inclusion in the models considering their biological relevance, based on previous knowledge of owl monkey dispersal, and social dynamics in other pair-living and socially monogamous taxa [12,49,62,63]. Tables with additional details and summaries of our data and model are presented in the electronic supplementary material. Datasets and code used in our analyses are reposited on FigShare [64]. Requests to use raw data for research purposes can be made to E.F.-D.

The first set of analyses examined general patterns of dispersal and how the 'age of dispersal' is related to competition over resources, evaluated through the social composition of the natal group. For this analysis, we chose 'group size', 'time since last birth', and 'adult replacement' as potential explanatory variables (table 2). We included group size and time since last birth because they may influence the amount of resource competition within a disperser's natal group. Since owl monkeys are pair-living, variation in group size is largely determined by the presence of infants or younger offspring. Adult replacements also are likely to influence social dynamics, particularly between adults and older individuals (juveniles and subadults), since non-related individuals can become competitors for food resources and present mating opportunities [12]. We did not include sex because age at dispersal is fairly similar for males and females [50,65] and sex was known for only 34% of offspring in the dataset (n = 112/325); thus, not including sex helps avoid overfitting. We used these variables to construct seven candidate Cox-proportional hazard models that considered censored data to explain the variation in age at dispersal (electronic supplementary material, table 2я). We removed individuals who died prior to reaching the minimum dispersal age (n = 75) and ran the seven candidate models on the remaining dataset (n = 173 individuals), censoring individuals still in their natal groups (n = 22). We also wanted to examine the effect that our method of categorizing dispersals, specifically including offspring that disappeared (i.e. presumed dispersal), may have on estimating age at dispersal. To do this, we ran the seven candidate models again using only confirmed dispersals (n = 46) (electronic supplementary material, table 2я).

The second set of analyses explored the potential influence of mate competition and inbreeding avoidance on dispersal by examining how adult replacements, which introduce a potential mate or mate competitor to the group, may influence the timing of dispersal. When a solitary floater displaces an adult in a group and becomes the new resident adult it probably changes social interactions between adults and offspring. Whether this new adult represents a potential mate, or a mate competitor, will depend on the young's age and sex [12,66]. Thus, we included 'age at replacement' and 'same-sex replacement' as potential explanatory variables. Females begin to develop mature hormone profiles prior to dispersing [67], but it is unknown if males become sexually mature while still in the natal group. We therefore also included the disperser's sex in interaction terms in this set of models. We constructed nine Cox-proportional hazard candidate models (electronic supplementary material, table 2b) to examine how explanatory variables related to how long an offspring remains in the natal group after experiencing a replacement ('time to dispersal'). We used data from the subset of individuals who experienced a replacement and had dates of birth and dispersal that could be estimated with an accuracy of at least six months (58 individuals: 32 presumed dispersals and 26 confirmed dispersals). Some individuals experienced more than one adult replacement. Since an individual can only disperse once, we only considered the one replacement that occurred most immediately before dispersal.

Since an adult replacement exposes offspring to an unrelated adult, older offspring who are undergoing sexual maturity (i.e. subadults) may perceive, or be perceived by, this new adult as a potential mating partner or mating competitor. We thus predicted that adult replacements would influence subadults differently from younger offspring. To test this prediction, we performed a separate analysis that included only the subset of individuals who were subadults (>24 months old) at the time of the replacement and whose genetic sex was known. Twenty-two individuals experienced, as subadults, the replacement of their same-sex parent (n = 4), opposite-sex parent (n = 8) or both parents (n = 7); the sex of three subadults whose sex was unknown were excluded from analyses. To avoid overfitting the data, we did not create candidate models for this comparatively smaller subset of data. Instead, we calculated the mean number of months that individuals who experienced the replacement of a same, or opposite, sex parent remained in the natal group after the replacement.

The third set of analyses investigated the influence of resource competition on the seasonality of dispersal. To attempt disentangling the potential influences of group composition changes associated with the birth season [68] and resource abundance we defined seasonality in two ways and performed separate analyses on each. First, we constructed 15 candidate generalized linear models for which the outcome variable was whether a dispersal occurred during the 'birth season', with a dataset of 210 individuals. 'Age at dispersal', 'group size', 'adult replacement' and 'recent birth' were included as potential explanatory variables (table 2; electronic supplementary material, table S2c). We did not use time since last birth, as in the other two sets of analyses, because births, being highly seasonal, would have been correlated with the outcome variable. Second, we constructed 15 candidate models for which the outcome variable was whether dispersal occurred during the dry 'winter season', when resource abundance and temperatures are lowest [69]. The 'dry season' of May-August is a period of limited food availability [59]; groups occupy territories that provide reliable dry season foods within the core areas [58]. Given that when offspring disperse they lose reliable access to resources in their natal group's core home range, these months of low food availability and low temperatures probably represent the time when dispersing and subsequently ranging solitarily is most difficult. We therefore designed our candidate models to examine which variables might explain why individuals sometimes disperse during the harshest time of the year. As potential explanatory variables, we included 'dispersal age', 'adult replacement', 'group size' and an estimate of food availability during the dry season, 'winter fruit abundance' (table 2; electronic supplementary material, table S2c). Our dataset for these models included 109 individuals from groups for which we were able to estimate winter fruit availability in the natal group's home range.

We performed statistical analyses in R v. 3.3.2 [70], using the package AICcmodavg (v. 2.1-0) to calculate model characteristics and model-averaged parameter estimates, their standard errors and 95% unconditional confidence intervals (table 3) [71]. We report the mean ± 1 s.d. unless otherwise specified.

3. Results

3.1. Float on: both males and females always disperse and avoid reproducing in their natal groups

Dispersal was an obligatory life-history stage. No individuals reproduced in the group where they were born (n = 337, 30 groups, 1997-2020, table 1). They all dispersed from their natal groups or died before having reproduced there. Of 319 offspring whose fates could be determined, 66% dispersed (n = 50 confirmed and n = 160 presumed), 26% died (n = 82) and 8% (n = 27) were still in their natal groups at the end of the study.

The age at dispersal was highly variable. Offspring whose age at dispersal was estimated to ±6 months dispersed when they were between 1.5 and 5 years old (18-60 months; median = 35 months; mean ± s.d. = 34.5 ± 9.1 months). Hence, some offspring dispersed before the onset of sexual maturity, while others stayed well after it [67].

Males and females did not differ much in their ages of dispersal (median (mean ± s.d.): males = 38 (36.6 ± 8.5) months, females = 37 (38.0 ± 8.7) months). Even though both sexes had similar probabilities of dispersing at most ages, the probabilities of dispersal were somewhat male-biased at earlier (28-35 months) and latest (50-60 months) ages (figure 1).

3.2. Size and composition of the natal group are not strongly associated with earlier dispersals

Dispersing individuals (n = 210) experienced variation in the size of their natal group, whether step-parents were present (i.e. a replacement had occurred), and whether there was a recently born sibling at the time they dispersed. The mean size of the natal groups was 4.2 ± 0.8 s.d. (range 3-7) including the dispersing individual, 31% (64/210) of them had lived with at least one step-parent, and a mean of 11.1 ± 9.3 s.d. months (range 0-46) had passed since the last infant was born in the natal group.

The time since an infant was born (last birth') was included in all four models that met the selection criteria (electronic supplementary material, table S2a). Specifically, an additional month since the last birth decreased the monthly chance of dispersal by 2% as indicated by the -0.02 model-averaged estimated effect of this variable (table 3). Having a step-parent in the group before dispersal ('adult replacement') and 'group size' were each included in two of the four models. Young in groups with step-parents had 35% less chance of dispersing at a given age than those who lived with their biological parents; and having a larger group size at the time of dispersal reduced the chance of dispersal by 30% (table 3). Confidence intervals (95% CI) for the hazard ratio of all three variables approach or include 1, indicating that evidence for the influence of these variables was not very robust. Sensitivity analyses conducted with a more conservative subset of the data (i.e. including only confirmed dispersals) also produced hazard ratios with 95% CI that included 1 (electronic supplementary material, table S3).

3.3. Mating competition: subadults are less likely to disperse if a potential mate joins the group

Losing a biological parent did not increase the probability of dispersal. About a third (31%, n = 64) of the 210 dispersing individuals were, at the time of dispersal, living with at least one step-parent. This situation occurred because one, or both, of their biological parents had been evicted from the group by a same-sex solitary floater [48]. Age at dispersal was similar for individuals living with at least one step-parent and those who had both biological parents present at the time of dispersal (mean ± s.d. for step-parent(s) versus biological parents: 36.1 ± 9.5 months versus 34.7 ± 8.7 months; n = 111). A more conservative analysis limited to confirmed dispersals produced similar results (39.8 ± 9.2 versus 39.7 ± 6.3 months; n = 45) (electronic supplementary material, figure S2). There was much variation in the temporal relationship between losing a biological parent and dispersing. Individuals left the natal group 0-39.7 months after their parent had been evicted (mean ± s.d.: 16.0 ± 10.5 months; 13.6 ± 9.5 months if only the most recent replacement is considered for individuals who experienced multiple replacements). There was little difference in the mean age at dispersal for those who had lost their biological mother (36.9 ± 9.2 s.d.) or father (36.4 ± 8.5 s.d.); and in the time to dispersal since the replacement (mothers versus fathers: 14.5 ± 10.7 months versus 17.5 ± 10.1 months; electronic supplementary material, figure S3fl). This was also true when only subadults (age >24 months) were considered (subadults remained 6.3 ± 4.3 and 5.9 ± 6.0 months, after male and female replacements, respectively; electronic supplementary material, figure S3b).

The models indicate that the age when an individual experienced a replacement and the sex of the adult being replaced, relative to the individual, were important factors for explaining the time that offspring remained in the natal group. Age at replacement' was the only variable included in all five models that met the criteria to explain the probability of dispersal if a potential mate joins the group, and it was the only variable included in the best model (electronic supplementary material, table S2b). Specifically, the hazard of dispersing increased 1.1 times for each additional month of age at the time a new adult moved into the group. Whether the new adult was of the 'same sex' as the dispersing individual, or not, was in three of the five best models. Offspring who experienced the replacement of a parent by a potential mate remained in the natal group longer, as indicated by the averaged model estimates (HR = 2.12; table 3). The sex of the dispersing individual was present only as an interaction term, but not on its own, in any of the five models and did not explain much variance in time to dispersal (electronic supplementary material, table S2b).

While the sex of a subadult, on its own, did not explain much of the variance in time to dispersal, the sex of the dispersing individual, relative to the sex of the parent that was replaced, was strongly associated. Specifically, the timing of a subadult's dispersal varied in relation to whether the new adult in the group was a potential mate (i.e. opposite sex as the subadult) or a potential mate competitor (i.e. same sex as the subadult). Individuals who lived with a step-parent as subadults (i.e. >24 months; n = 19) dispersed later when their opposite sex-parent had been replaced by a potential mate than when the same-sex parent had been replaced (mean months to dispersal ± s.d.: 7.2 ± 5.5 versus 2.3 ± 2.2; figure 2). Furthermore, 7 of the 8 subadults that had their same-sex parent replaced dispersed within four months, while more than half (6/10) of those that experienced the replacement of an opposite-sexed parent with a potential mate remained in the natal group for more than nine months (figure 2).

3.4. Resource competition: dispersal is more likely when food conditions are better

Dispersals occurred in all months. Still, they were concentrated during the austral spring season (93/210; figure 3; electronic supplementary material, figure S4). They occurred more frequently in spring than expected if they had randomly occurred throughout the year (44% versus 32%, proportion test = χ² = 6.99, d.f. = 1, p-value = 0.008; 95% CI: 0.03-0.22). They peaked markedly in October (n = 33), happening nearly twice as frequently than expected by chance (16% versus 8%). Only 29 individuals dispersed in the harsh late-autumn/winter period (May-August), accounting for 20% of dispersals, compared with the 34% expected by chance (χ² = 7.52, d.f. = 1, p-value = 0.006; 95% CI: -0.24 to -0.041; prop 1: 0.20; prop 2: 0.34). They were the least frequent in April and May (figure 3). These seasonal patterns of dispersal, which were similar for males and females (electronic supplementary material, figure 54a), also held when the analyses were done on only confirmed dispersal (electronic supplementary material, figure S4b).

Age at dispersal was very similar for those who dispersed in the spring season or some other time (mean ± s.d.: 34.7 ± 8.8 months versus 35.9 ± 12.9 months, n = 210), and in the harsh winter or in some other time (34.6 ± 12.0 months versus 34.8 ± 8.9 months, n = 148; electronic supplementary material, figure S5).

Models examining which variables may be related to dispersing during the spring season, when group composition usually changes and environmental conditions are more favourable, also indicate that age at dispersal is not strongly associated with the seasonality of dispersal. None of the four explanatory variables were strongly associated with spring season dispersals (table 3). Adult replacement7 increased the chance of dispersing during the birth season 1.6 times, but the 95% confidence intervals for this coefficient estimate included 1. If a birth had occurred in the natal group within the past year, the chance of dispersing during the birth season decreased by 60%, though the 95% confidence intervals for this hazard ratio estimate also included 1. While age at dispersal and group size were each included in at least 2 of the 5 models selected for averaging (electronic supplementary material, table S2c), both variables had averaged coefficients near 0, and corresponding hazard ratios of 1, indicating that neither was important in explaining whether dispersals occurred in the spring season.

The prediction that resource competition influences dispersal is not supported. The mean age at dispersal was very similar for individuals who dispersed in the winter and those who did it at other times of the year (mean ± s.d., age at dispersal: 34.6 ± 8.9 months versus 34.8 ± 12.0 months; electronic supplementary material, figure S5). Likewise, the mean amount of winter fruit available during the year of dispersal was also similar for individuals dispersing during winter and in other seasons (electronic supplementary material, figure S6). In the models, winter fruit abundance and age at dispersal explained almost none of the variability of winter season dispersals (table 3), as both had hazard ratios of 1. Of the 15 candidate models that met the selection criteria, only seven accounted for more than 5% of the cumulative weight (electronic supplementary material, table S2c).

In agreement with previous results on the influence of having an unrelated adult in the group on the probability of dispersal during the birth season (mid-September to early January), models indicated that individuals who lived with an unrelated adult were 37% less likely to disperse between May and August. Though the 95% confidence intervals for the hazard ratio for adult replacement included 1, replacements were substantially less frequent for individuals dispersing in winter than for those doing it in other seasons (32% (8/28) versus 42.5% (48/118)). On the other hand, more individuals dispersing in the birth season (35.9%, 33/92) had experienced a replacement than those that dispersed outside the birth season (26.7%, 31/116).

4. Discussion

Even when there was much variation in the age and timing of owl monkey dispersal one finding was very consistent across generations and 25 years of observations. Both males and females always dispersed and they never reproduced in their natal groups.

We predicted that if inbreeding avoidance was the primary cause of dispersal, then dispersals would consistently occur before, or around, the time individuals reach sexual maturity (approximately 3 years). The variation in age at dispersal indicates that while some individuals of both sexes dispersed around the time they reached sexual maturity, others delayed dispersal for up to 2 years [67,72]. While 31% of individuals had an unrelated adult (i.e. a potential mate) replace a genetic parent, the remaining 69% resided in natal groups with only close kin until they dispersed. These findings imply that, even when serial monogamy occurs, inbreeding is still a risk for the majority of owl monkeys who remain in the group after having reached sexual maturity. Thus, inbreeding avoidance does not, on its own, explain well the timing or age of dispersal in owl monkeys, but it is important in explaining why all individuals dispersed prior to reproducing.

We predicted that if mating competition was an important driver of dispersal, then the timing of dispersals would be influenced by adult replacements, but that the context of these replacements (i.e. age when they were experienced by the offspring) would be important [12]. As predicted, we found that adult replacements that occurred while offspring were young (<24 months), did not seem to be associated with earlier age at dispersal. Similarly, if the age when an offspring experienced an adult replacement was not taken into consideration, then having an adult of either sex replaced by a step-parent was not associated with leaving the natal group sooner (table 3). In contrast, for older offspring who had already undergone, or were close to the age of sexual maturity (i.e. subadults), the introduction of an unrelated step-parent was associated with the timing of dispersal, though this sample size was relatively small (n = 19). Specifically, when the replacement introduced an adult of the opposite sex (a potential mate), then owl monkeys remained in their natal groups longer than when the replacement introduced an adult of the same sex (a potential mate competitor) (figure 2). This result could signify that owl monkeys may be delaying dispersal to retain access to a new potential mate. However, this decision exposes them to mate competition with their same-sex genetic parent and we did not observe any successful cases of reproduction with step-parents. An alternative explanation is that owl monkeys may remain in their natal group longer when an opposite-sex parent is replaced because their remaining same-sex genetic parent may be more tolerant of them, compared with groups in which the same-sex parent is replaced. If mating competition with kin was driving dispersal, we would expect to see the opposite pattern (subadults dispersing sooner when the opposite-sex parent is replaced). Since owl monkeys disperse sooner after a same-sex adult enters their natal group, mating competition with new, unrelated adults that enter the group seems to play a greater role in triggering dispersal than mating competition with kin.

It is also important to note that just because subadults do not disperse (i.e. are not kicked out by their same-sex parent) when a potential unrelated mate is introduced, this does not mean that they are not being perceived as a potential mate competitor by their same-sex parent. Adults may tolerate subadults and allow them to remain in the group, but use behavioural mechanisms to prevent them from actually engaging in sexual behaviours (i.e. behavioural reproductive suppression). Specifically, adults may mate guard their partner, or act aggressively towards subadults, to prevent them from mating with the new unrelated individual [73,74]. It is also possible that a new adult entering the group may not perceive the subadult as a high-quality mating partner and prefer to mate with the resident adult over the subadult. In this case, the subadult may not actually be perceived by the same-sex parent as a viable mate competitor.

Owl monkey dispersals are highly seasonal, mostly occurring during the spring months when food abundance is high and temperatures are relatively warm (figure 3). This hints at individuals timing their dispersals to begin ranging solitarily, and looking for a mating position, when conditions are mild. October, in particular, may be an ideal time for individuals to disperse, because it is at the beginning of the spring/rainy season, giving individuals the maximum amount of time to float and attempt to acquire membership in a new group while the thermoregulatory challenges of being a solitary are minimal [69]. On the other hand, the variables associated with resource competition that we predicted to influence whether owl monkeys dispersed in winter, outside of this 'ideal', mild season, did not explain much of the variation. Resource competition with natal group members should be most severe during the winter, the harshest time of the year. Thus, if resource competition influenced dispersal, we would expect individuals to disperse more frequently during months when less food is available (i.e. when perceived resource competition is most intense). The prediction is not supported by our analyses: winter fruit abundance explained almost none of the variability of winter season dispersals (table 3). Owl monkeys' dietary flexibility may allow them to shift to consuming more leaves, or other food items, when fruit abundance is lower, which might explain why we did not find evidence of increased food competition or more dispersals during harsher winters. This is consistent with previous work documenting that owl monkey groups' home ranges produce consistent food resources, even during harsh winters [58].

Age of dispersal, group size or recent births did not explain much of the variability in the seasonality of dispersals (table 3). Both the intensity of food competition and the costs of dispersing and ranging solitarily vary throughout the year, as food availability and climatic conditions change. If, as we predicted, age, through its relationship to a larger body size [75], influenced the level of food competition with natal group members and/or how costly it would be for dispersers to leave the natal group/territory, then we would expect the season in which an individual dispersed to be strongly associated to the disperser's age. However, age at dispersal was very similar for those who dispersed in the spring season or some other time and in the harsh winter or in some other time (table 3; electronic supplementary material, figure S5).

Thus, overall, the third set of models did not provide much insight into why certain individuals may disperse outside of the expected dispersal season (spring/birth period), or why some even disperse during the harshest months (May-August). The results of these models are supported by plots (electronic supplementary material, figures S5 and S6) showing that dispersers had similar means and levels of variation for age and winter fruit abundance, whether or not they dispersed within the birth season or winter season. Adult replacements may play some role in explaining seasonality of dispersal: our third set of models indicated that adult replacement was associated with a greater likelihood of dispersing during the birth season and a reduced likelihood of dispersing during the winter, but confidence intervals for this effect were large (table 3). It remains unclear why experiencing an adult replacement may make an individual more likely to disperse during the spring/birth season, when conditions are likely most favourable for newly dispersed individuals to range solitarily. One possibility is that the introduction of a non-related adult reduces the nepotistic benefits of philopatry [76,77]. If so, offspring that reside with genetic parents may continue to delay dispersal, owing to potential philopatric benefits associated with remaining near close kin [78,79], whereas those that experience the replacement of a genetic parent with an unrelated step-parent may choose to disperse when conditions are relatively good.

4.1. Limitations and future directions

As is the case with all data analyses, we had to make decisions about which variables to include and which subsets of individuals to use in the models, which may have influenced our results. In all cases, we used prior knowledge of owl monkey biology and social systems to perform quality control on the data and select the most biologically relevant variables for the candidate models. Nonetheless, it is likely that variables we were unable to measure, such as body condition or the small-scale abundance of resources, including foods other than fruit, may be important in explaining at least some of the variation in dispersal that we observed.

As with many studies of dispersal, we were limited by our ability to follow individuals who dispersed outside of our study area, which may have influenced our findings. To evaluate the robustness of our results, we performed several sensitivity analysis exercises (electronic supplementary material). For example, including censored individuals still in their natal group, or individuals who had disappeared (presumed dispersals), rather than limiting analyses to confirmed dispersals, had little influence on the magnitude of the effect or hazard ratio and never changed the sign of the estimated effect. Likewise, estimates of our models examining potential causes of winter dispersals (Set 3b) were very similar when we included all individuals and when only the subset of offspring that remained in their natal group until the onset of winter were included (electronic supplementary material, table S3).

We did not include information on what happened to individuals after they dispersed in the analyses. This was because these data are even more challenging to obtain and therefore were not available for the majority of dispersing individuals. However, knowing the fates of individuals who disappear from their natal groups could be important for evaluating biological and evolutionary interpretations of the variation in age and timing of dispersal that we observed. Including presumed dispersals did result in a somewhat earlier mean age at dispersal, compared with the estimate when only confirmed dispersals were considered (electronic supplementary material, figure SI). This suggests that at least some of the individuals who we presumed to have dispersed may actually have disappeared because they died while still in their natal groups, rather than successfully dispersing. While there was a lot of variation in the age and time of year of dispersal, it may be the case that there is an optimal range of ages, or ecological conditions, for it (i.e. individuals who disperse at ideal times or under optimal conditions have a much greater chance to successfully find a breeding position and reproduce). Exploring how the age and timing of dispersal are associated with the amount of time spent as a floater before finding a mate, and ultimately with life-time reproductive success, are important future avenues of investigation. Finally, all the data in our study came from a single location, where territories appear to be saturated. It is unclear to what extent the patterns we observed may be generalizable to other taxa living in different ecological conditions. Future studies that include additional populations, or other Aotus species in different environments, would allow us to better assess associations between dispersal patterns and ecological variation through a comparative approach [73].

In summary, in Azara's owl monkey dispersal is a definite life event, but its timing is flexible. To some extent, inbreeding avoidance and competition over food and potential mates in the natal group all appear to contribute to regulating dispersal, though the relative importance of each factor is context dependent. Our results emphasize that the avoidance of inbreeding, mate competition and resource competition are non-exclusive: these factors may work together to shape the patterns of dispersal.

Ethics. All research protocols reported in this paper were reviewed and approved by an appropriate institution and/or governmental agency that regulates research with animals. Specifically, all research reported complied with the protocols approved by the Institutional Animal Care and Use Committees of the Zoological Society of San Diego (2000-2005), the University of Pennsylvania (2006-2014) and Yale University (2014-present). This research also received clearance from, and complied with, guidelines approved by the National Wildlife Directorate in Argentina and the Argentine Society for Mammalian Studies, and adhered to the legal requirements of the government of Argentina.

Data accessibility. All data files and scripts associated with analyses reported in this paper are available in the FigShare repository, which can be accessed with the following link: https://figshare.eom/s/a97eb4b3ef9cb5c66d55.

Supplementary material is available online [80].

Declaration of Al use. We have not used Ai-assisted technologies in creating this article.

Authors7 contributions. M.C.: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, writing-original draft, writing-review and editing; A.G.d.l.C.: conceptualization, investigation, writing-review and editing; G.v.d.H.: formal analysis, methodology, writing-review and editing; M.R.: data curation, investigation; A.C.: funding acquisition, resources, writing-review and editing; E.F.-D.: conceptualization, data curation, funding acquisition, investigation, methodology, project administration, resources, writing- review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Conflict of interest declaration. We declare we have no competing interests.

Funding. Fieldwork leading to the data summarized here was supported through grants to E.F.-D. from the Wenner-Gren Foundation, L. S. B. Leakey Foundation, National Geographic Society, National Science Foundation (NSF-BCS-0621020, 1232349, 1503753, 1848954; RAPID-1219368; NSF-REU 0837921, 0924352, 1026991) and the National Institutes of Aging (NIA-P30 AG012836-19, NICHD R24 HD-044964-11). M.C. acknowledges financial support from the University of Pennsylvania, Leakey Foundation, International Primatological Society, American Society of Primatology, Nacey Maggioncalda Foundation and National Science Foundation (DDRIG-1540255). A.G.d.l.C. acknowledges support from the L. S. B. Leakey Foundation and the National Geographic Society (EC-54383R-18). The OMP also received institutional support from the Zoological Society of San Diego, the University of Pennsylvania and Yale University.

Acknowledgements. We are grateful to the Argentinean government and the Province of Formosa for permission to conduct our research, and to Bellamar Estancias and Fundación ECO for their support. Our research would not have been possible without the help of the more than 300 students and volunteers who over the years have provided research assistance in the field, particularly those who were involved in aspects of collecting dispersal data research during several years: Cecilia Juárez and Victor Davalos. We are also grateful to Paul Babb (UPenn), and Carol Mariani and Evelyn Jensen (Yale), who provided assistance and guidance in the development of protocols for the extraction and genotyping work, and Jeffrey Rogers and colleagues (Baylor College of Medicine) for providing A. azarae genomic data used to develop our microsatellite markers.

Sidebar

Cite this article: Corley M, Garcia de la Chica A, van der Heide G, Rotundo M, Caccone A, Fernandez-Duque E. 2024 Inbreeding avoidance, competition and natal dispersal in a pair-living, genetically monogamous mammal, Azara's owl monkey (Aotus azarae). R. Soc. Open Sci. 11 : 240379.

https://doi.org/10.1098/rsos.240379

Received: 7 March 2024

Accepted: 25 June 2024

Subject Category:

Organismal and evolutionary biology

Subject Areas:

behaviour, ecology

Author for correspondence:

Alba Garcia de la Chica

e-mail: [email protected]

References

References

1. Bonte D, Dahirel M. 2017 Dispersal: a central and independent trait in life history. Oto 126,472-479. (doi:10.1111/oik.03801 )

2. Clobert J, Danchin E, Dhondt AA, Nichols JD. 2001 Dispersal. Oxford, UK: Oxford University Press.

3. Bonte D et al. 2012 Costs of dispersal. Biol. Rev. Camb. Philos. Soc. 87,290-312. (doi:10.1111/j.1469-185X.2011.00201.x)

4. Doligez B, Part T. 2008 Estimating fitness consequences of dispersal: a road to 'know-where'? Non-random dispersal and the underestimation of dispersers' fitness. J. Anim. Ecol. 77,1199-1211. (doi: 10.1111 /j. 1365-2656.2008.01446.x)

5. Ekman J. 2007 Delayed dispersal: youth costs carry lifetime gains. Curr. Biol. 17, R417-8. (doi:10.1016/j.cub.2007.04.002)

6. Strier KB, Possamai CB, Mendes SL 2015 Dispersal patterns of female northern muriquis: implications for social dynamics, life history, and conservation. In Dispersing primate females: life history and social strategies in male-philopatric species (eds T Furuichi, J Yamagiwa, F Aureli), pp. 3-22. Tokyo, Japan: Springer. (doi:10.1007/978-4-431-55480-6J)

7. Hamilton WD. 1964 The genetical evolution of social behaviour./ Theor. Biol. 7,1-16. (doi:10.1016/0022-5193(64)90038-4)

8. Fernandez-Duque M, Chapman CA, Glander KE, Fernandez-Duque E. 2018 Darting primates: steps toward procedural and reporting standards. Int. J. Primato!. 39,1009-1016. (doi:10.1007/s10764-017-9963-z)

9. Clobert J, Le Galliard JF, Cote J, Meylan S, Massot M. 2009 Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol. Lett. 12,197-209. (d o i : 10.1111 /j. 1461 -0248.2008.01267.x)

10. Reinke BA, Miller DAW, Janzen FJ. 2019 What have long-term field studies taught us about population dynamics? Annu. Rev. Ecol. Evol. Syst. 50, 261-278. (doi:10.1146/annurev-ecolsys-110218-024717)

11. Stephen Dobson F. 1982 Competition for mates and predominant juvenile male dispersal in mammals. Anim. Behav. 30,1183-1192. (doi:10. 1016/S0003-3472(82)80209-1)

12. Emlen ST. 1997 Predicting family dynamics in social vertebrates. In Behavioural ecology: an evolutionary approach (eds JR Krebs, NB Davies), pp. 228-253. Malden, MA: Blackwell Sciences.

13. Greenwood PJ. 1980 Mating systems, philopatry and dispersal in birds and mammals. Anim. Behav. 28,1140-1162. (doi:10.1016/S0003-3472(80)80103-5)

14. Lawson Handley LJ, Perrin N. 2007 Advances in our understanding of mammalian sex-biased dispersal. Mol. Ecol. 16,1559-1578. (doi:10.1111/ j.1365-294X.2006.03152.x)

15. Trakhtenbrot A, Nathan R, Perry G, Richardson DM. 2005 The importance of long-distance dispersal in biodiversity conservation. Divers. Distrib. 11,173-181. (doi:10.1111/j.1366-9516.2005.00156.x)

16. Travis JMJ et al. 2013 Dispersal and species' responses to climate change. Oikos 122,1532-1540. (d o i : 10.1111 /j. 1600-0706.2013.00399.x)

17. Tucker MA et al. 2018 Moving in the Anthropocene: global reductions in terrestrial mammalian movements. Science 359,466-469. (doi:10. 1126/science.aam9712)

18. Greenwood PJ. 1983 Mating systems and the evolutionary consequences of dispersal. In The ecology of animal movement (eds IR Swingland, PJ Greenwood), pp. 116-131. Oxford, UK: Clarendon Press.

19. Nagy M, Heckel G, Voigt CC, Mayer F. 2007 Female-biased dispersal and patrilocal kin groups in a mammal with resource-defence polygyny. Proc. R. Soc. B 274,3019-3025. (doi:10.1098/rspb.2007.1008)

20. Wolff JO. 1994 More on juvenile dispersal in mammals. Oto 71,349. (doi:10.2307/3546284)

21. Di Fiore A, Rendall D. 1994 Evolution of social organization: a reappraisal for primates by using phylogeneby using phylogenetic methods. Proc. Natl Acad. Sei. USA 91,9941-9945. (doi:10.1073/pnas.91.21.9941)

22. Mabry KE, Shelley EL, Davis KE, Blumstein DT, Van Vuren DH. 2013 Social mating system and sex-biased dispersal in mammals and birds: a phylogenetic analysis. PLoS One 8, e57980. (doi: 10.1371 /journal.pone.0057980)

23. Perrin N, Mazalov V. 1999 Dispersal and inbreeding avoidance. Am. Nat. 154,282-292. (doi:10.1086/303236)

24. Murren CJ, Julliard R, Schlichting CD, Clobert J. 2001 Dispersal, individual phenotype, and phenotypic plasticity. New York, NY: Oxford University Press.

25. Travis JMJ etai. 2012 Modelling dispersal: an eco-evolutionary framework incorporating emigration, movement, settlement behaviour and the multiple costs involved. Methods Ecol. Evol. 3,628-641. (doi:10.1111/j.2041-210X.2012.00193.x)

26. Trochet A, Courtois EA, Stevens VM, Baguette M, (haine A, Schmeller DS, Clobert J, Irschick DJ, Wiens JJ. 2016 Evolution of sex-biased dispersal. Q. Rev. Biol. 91,297-30. (doi:10.1086/688097)

27. Johnson ML, Gaines MS. 1990 Evolution of dispersal: theoretical models and empirical tests using birds and mammals. Annu. Rev. Ecol. Syst. 21, 449-480. (doi:10.1146/annurev.es.21.110190.002313)

28. Kokko H, Lundberg P. 2001 Dispersal, migration, and offspring retention in saturated habitats./Im. Nat. 157,188-202. (doi:10.1086/318632)

29. Perrin N, Mazalov V. 2000 Local competition, inbreeding, and the evolution of sex-biased dispersal. Am. Nat. 155,116-127. (doi:10.1086/303296)

30. Clutton-Brock TH. 1989 Female transfer and inbreeding avoidance in social mammals. Nature 337,70-72. (doi:10.1038/337070a0)

31. Pusey AE, Packer C. 1987 Dispersal and philopatry. In Primate societies, pp. 250-266. Chicago, IL: University of Chicago Press.

32. Pusey A, Wolf M. 1996 Inbreeding avoidance in animals. Trends Ecol. Evol. (AmstJU, 201-206. (doi:10.1016/0169-5347(96) 10028-8)

33. Galezo AA et al. 2022 Mechanisms of inbreeding avoidance in a wild Primate. Curr. Biol. 32,1607-1615.(doi:10.1016/j.cub.2022.01.082)

34. Pike VL, Cornwallis CK, Griffin AS. 2021 Why don't all animals avoid inbreeding? Proc. R. Soc. B 288, 20211045. (doi:10.1098/rspb.2021.1045)

35. Brooked MG, Rowley I, Adams M, Baverstock PR. 1990 Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species. Behav. Ecol. Sociobiol. 26,191-199. (doi:10.1007/BF00172086)

36. Brouwer L, Van De Pol M, Atema E, Cockburn A. 2011 Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopaegic. Mol. Ecol. 20,4796-4807. (doi:10.1111 /j.1365-294X.2011.05325.x)

37. Ekman J, Dickinson JL, Hatchwell BJ, Griesser M. 2004 Delayed dispersal. In Ecology and evolution of cooperative breeding in birds (eds WD Koenig, JL Dickinson), pp. 48-66. Cambridge, UK: Cambridge University Press. (doi:10.1017/CB09780511606816)

38. Emlen ST. 1982 The evolution of helping. I. An ecological constraints model./Im. Nat. 119,29-39. (doi:10.1086/283888)

39. Marjamaki PH, Contasti AL, Coulson TN, McLoughlin PD. 2013 Local density and group size interacts with age and sex to determine direction and rate of social dispersal in a polygynous mammal. Ecol. Evol. 3,3073-3082. (doi:10.1002/ece3.694)

40. Pasinelli G, Walters JR. 2002 Social and environmental factors affect natal dispersal and philopatry of male red-cockaded woodpeckers. Ecology 83,2229-2239. (doi:10.1890/0012-9658(2002)083[2229:SAEFAN]2.0.C0;2)

41. Quirici V, Faugeron S, Hayes LD, Ebensperger LA. 2011 The influence of group size on natal dispersal in the communally rearing and semifossorial rodent, Octodon degus. Behav. Ecol. Sociobiol. 65,787-798. (doi:10.1007/s00265-010-1082-1)

42. VanderWaal KL, Mosser A, Packer C. 2009 Optimal group size, dispersal decisions and postdispersal relationships in female African lions. Anim. Behav. 77,949-954. (doi:10.1016/j.anbehav.2008.12.028)

43. Sheldon BC, Kruuk LEB, Alberts SC. 2022 The expanding value of long-term studies of individuals in the wild. Nat. Ecol. Evol. 6,1799-1801. (doi: 10.1038/S41559-022-01940-7)

44. Huck M, Fernandez-Duque E. 2017 The floater's dilemma: use of space by wild solitary Azara's owl monkeys (Aotus azarae) in relation to group ranges. Anim. Behav. 127,33-41. (doi:10.1016/j.anbehav.2017.02.025)

45. Ronce 0.2007 How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu. Rev. Ecol. Evol. Syst. 38,231-253. (doi: 10.1146/annurev.ecolsys.38.091206.09561l)

46. Huck M, Fernandez-Duque E, Babb P, Schurr T. 2014 Correlates of genetic monogatic monogamy in socially monogamous mammals: insights from Azara's owl monkeys. Proc. R. Soc. B 281,20140195. (doi:10.1098/rspb.2014.0195)

47. Fernandez-Duque E. 2012 Owl monkeys Aotus spp in the wild and in captivity. Int. Zoo Yearbook 46, 80-94. (doi:10.1111/j.1748-1090.2011. 00156.x)

48. Fernandez-Duque E, Huck M. 2013 Till death (or an intruder) do us part: intrasexual-competition in a monogamous primate. PLoS One 8, e53724. (doi:10.137l/journal.pone.0053724)

49. HuckM, Fernandez-Duque E. 2012 Children of divorce: effects of adult replacements on previous offspring in Argentinean owl monkeys. Behav. Ecol. Sociobiol. 66,505-517. (doi:10.1007/s00265-011-1297-9)

50. Fernandez-Duque E. 2009 Natal dispersal in monogamous owl monkeys (Aotus azara!) of the Argentinean Chaco. Behaviour 146,583-606. (doi: 10.1163/156853908X397925)

51. Fernandez-Duque E, Huntington C. 2002 Disappearances of individuals from social groups have implications for understanding natal dispersal in monogamous owl monkeys (Aotusazarai).Am.J. Primatol. 57,219-225. (doi:10.1002/ajp.10045)

52. Fernandez-Duque E, Rotundo M, Sloan C. 2001 Density and population structure of owl monkeys (Aotus azara!) in the Argentinean Chaco. Am. J. Primatol. 53,99-108. (doi:10.1002/1098-2345(200103)53:3<99:AID-AJP1>3.0.C0;2-N)

53. Fernandez-Duque E. 2016 Social monogamy in wild owl monkeys (Aotus azarae) of Argentina: the potential influences of resource distribution and ranging patterns. Am J. Primatol. 78,355-371. (doi:10.1002/ajp.22397)

54. Juarez CP, Rotundo MA, Berg W, Fernández-Duque E. 2011 Costs and benefits of radio-collaring on the behavior, demography, and conservation of owl monkeys (Aotus azara!) in Formosa, Argentina. Int. J. Primatol. 32,69-82. (doi:10.1007/s10764-010-9437-z)

55. Fiore AD. 2006 A rapid genetic method for sex assignment in non-human primates. Conserv. Genet. 6,1053-1058. (doi:10.1007/S110592-005-9086-5) 9086-5)

56. Kuderna LFK etai. 2023 A global catalog of whole-genome diversity from 233 primate species. Science 380, 906-913. (doi:10.1126/science. abn7829)

57. Schuelke M. 2000 An economic method for the fluorescent labeling of PCR fragments. Nat. Biotechnol. 18,233-234. (doi:10.1038/72708)

58. Fernandez-Duque E, van der Heide G. 2013 Dry season resources and their relationship with owl monkey (Aotus azarae) feeding behavior, demography, and life history. Int. J. Primatol. 34,752-769. (doi:10.1007/s10764-013-9689-5)

59. van der Heide G, Fernandez-Duque E, Hart D, Juárez CP. 2012 Do forest composition and fruit availability predict demographic differences among groups of territorial owl monkeys (Aotus azarai)! Int. J. Primatol. 33,184-207. (doi:10.1007/s10764-011-9560-5)

60. Burnham KP, Anderson D. 2002 Model selection and multi-model inference. New York, NY: Springer-Verlag.

61. Symonds MRE, Moussalli A. 2011 A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Bebav. Ecol. Sociobiol. 65,13-21. (doi:10.1007/s00265-010-1037-6)

62. Eikenaar C, Richardson DS, Brouwer L, Komdeur J. 2007 Parent presence, delayed dispersal, and territory acquisition in the Seychelles warbler. Bebav. Ecol. 18,874-879. (doi:10.1093/beheco/arm047)

63. Piper WH, Slater G. 1993 Polyandry and incest avoidance in the cooperative stripe-backed wren of Venezuela. Behaviour 124,227-247. (doi:10. 1163/156853993X00597)

64. Corley M, Garcia de la Chica A, van der Heide G, Rotundo M, Caccone A, Fernandez-Duque E. 2024 Associations between inbreeding avoidance, competition, and dispersal in a pair-living, genetically monogamous mammal, Azara's owl monkey (Aotus azarae). See https://figshare.eom/s/ a97eb4b3ef9cb5c66d55.

65. Corley M. 2017 Leaving home: demographic, endocrine, and behavioral correlates of dispersal in monogamous owl monkeys (aotus azarae) of argentina. Doctoral dissertation, University of Pennsylvania, Philadelphia, PA, USA. https://www.proquest.com/dissertations-theses/leaving-home-demographic-endocrine-behavioral/docview/1927710700/se-2?accountid=15172.

66. Emlen ST. 1995 An evolutionary theory of the family. Proc. Natl Acad. Sci. USA 92,8092-8099. (doi:10.1073/pnas.92.18.8092)

67. Corley M, Valeggia C, Fernandez-Duque E. 2017 Hormonal correlates of development and natal dispersal in wild female owl monkeys (Aotus azarae) of Argentina. Borm. Bebav. 96,42-51. (doi:10.1016/j.yhbeh.2O17.08.005)

68. Fernandez-Duque E, Rotundo M, Ramirez-Llorens P. 2002 Environmental determinants of birth seasonality in night monkeys (Aotus azarai) of the Argentinean Chaco. Int. J. Primatol. 23,639-656. (doi:10.1023/A: 1014929902923)

69. Perea-Rodriguez JP, de la Iglesia H, Fernandez-Duque E. 2023 What owl monkeys (Aotus spp.) tell us about the dynamics between thermoenergetics and organismal biology. In Owl monkeys: evolution, behavioral ecology and conservation (ed. E Fernandez-Duque), pp. 301-321. Cham, Switzerland: Springer. (doi:10.1007/978-3-031-13555-2_10)

70. R Core Development Team. 2021 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

71. Mazerolle MJ. 2019 Package 'Aiccmodavg.

72. Corley M, Spence-Aizenberg A, Fernandez-Duque E, Valeggia C. 2023 Reproductive ecology and behavioral endocrinology of owl monkeys. In Owl monkeys: evolution, behavioral Ecology and conservation (ed E Fernandez-Dugue). Springer.

73. Corley M, Fernandez-Duque E. 2023 Dispersal: a critical life-history stage influencing populations, social dynamics, and individual fitness. In Owl monkeys: evolution, behavioral ecology and conservation (ed. E Fernandez-Duque), pp. 423-459. Cham, Switzerland: Springer. (doi:10.1007/ 978-3-031-13555-2_15)

74. Corley MK, Xia S, Fernandez-Duque E. 2017 The role of intragroup agonism in parent-offspring relationships and natal dispersal in monogamous owl monkeys (Aotus azarae) of Argentina./Im J. Primato!. 79, e22712. (doi:10.1002/ajp.22712)

75. Huck M, Rotundo M, Fernandez-Duque E. 2011 Growth and development in wild owl monkey (Aotus azarai) of Argentina. Int. J. Primatol. 32, 1133-1152. (doi: 10.1007/s 10764-011 -9530-y)

76. Ekman J, Baglione V, Eggers S, Griesser M. 2001 Delayed dispersal: living under the reign of nepotistic parents. Auk 118,1-10. (doi:10.1093/ auk/118.1.1)

77. Kokko H, Ekman J. 2002 Delayed dispersal as a route to breeding: territorial inheritance, safe havens, and ecological constraints. Am. Nat. 160, 468-484. (doi:10.1086/342074)

78. Nelson-Flower MJ, Wiley EM, Flower TP, Ridley AR. 2018 Individual dispersal delays in a cooperative breeder: ecological constraints, the benefits of philopatry and the social queue for dominance. J. Anim. Ecol. 87,1227-1238. (doi:10.1111/1365-2656.12814)

79. Mayer M, Zedrosser A, Rosell F. 2017 When to leave: the timing of natal dispersal in a large, monogamous rodent, the Eurasian beaver. Anim. Behav. 123,375-382. (doi:10.1016/j\anbehav.2O16.11.020)

80. CorleyM, Garcia de la Chica A, van der Heide G et al. 2024 Data from: Inbreeding avoidance, competition and natal dispersal in a pair-living, genetically monogamous mammal, azara's owl monkey (Aotus azarae). Figshare. (doi:10.6084/m9.figshare.c.7389787)