Vascularization underlies differences in sexually selected skin coloration in a wild primate.

Male reproductive competition can select for condition-dependent, conspicuous traits that signal some aspect of fighting ability and facilitate assessment of potential rivals. However, the underlying mechanisms that link the signal to a male's current condition are difficult to investigate in wild populations, often requiring invasive experimental manipulation. Here, we use digital photographs and chest skin samples to investigate the mechanisms of a visual signal used in male competition in a wild primate, the red chest patch in geladas (Theropithecus gelada). We analysed photographs collected during natural (n = 144) and anaesthetized conditions (n = 38) to understand variability in male and female chest redness, and we used chest skin biopsies (n = 38) to explore sex differences in gene expression. Male and female geladas showed similar average redness, but males exhibited a wider within-individual range in redness under natural conditions. These sex differences were also reflected at the molecular level, with 10.5% of genes exhibiting significant sex differences in expression. Subadult males exhibited intermediate gene expression patterns between adult males and females, pointing to mechanisms underlying the development of the red chest patch. We found that genes more highly expressed in males were associated with blood vessel development and maintenance but not with androgen or oestrogen activity. Together, our results suggest male gelada redness variability is driven by increased blood vessel branching in the chest skin, providing a potential link between male chest redness and current condition as increased blood circulation to exposed skin could lead to heat loss in the cold, high-altitude environment of geladas.

A novel statovirus identified in fecal samples from wild geladas in the Ethiopian highlands.

We present a novel statovirus in geladas (Theropithecus gelada), graminivorous primates endemic to the Ethiopian highlands. Using a high-throughput sequencing approach, we identified contiguous sequences in feces from two adult female geladas in the Simien Mountains National Park, Ethiopia, that share similarities to statoviruses. Our phylogenetic analysis of the whole genome, as well as the RNA-dependent RNA polymerase (RdRp) and capsid protein (CP) amino acid sequences, revealed that the gelada statoviruses cluster with those from other primates (laboratory populations of Macaca nemestrina and Macaca mulatta). As the first report of statovirus in wild primates, this finding contributes to our understanding of the phylogenetic and geographic distribution of statoviruses and their hosts.

Leveling with Tinbergen: Four levels simplified to causes and consequences.

In 1963, Niko Tinbergen published his foundational manuscript identifying the four questions we ask in animal behavior-how does the behavior emerge across the lifespan (development); how does it work (mechanism); how and why did it evolve (evolution); and why is it adaptive (function). Tinbergen clarified that these 'levels of analysis' are complementary, not competing, thereby avoiding many fruitless scientific debates. However, the relationships among the four levels was never established. Here, we propose 'leveling' Tinbergen's questions to a single temporal timescale divided into causes (encompassing mechanism, development, and evolution) and consequences (encompassing function). Scientific advances now seamlessly link evolution, development, and mechanism into a continuum of 'causes'. The cause-consequence distinction separates the processes that precede (and lead to) a behavior, from the processes that come after (and result from) a behavior. Even for past behaviors, the functional outcomes are (historical) consequences of the causes that preceded them.

Using an on-site laboratory for fecal steroid analysis in wild white-faced capuchins.

Hormone laboratories located "on-site" where field studies are being conducted have a number of advantages. On-site laboratories allow hormone analyses to proceed in near-real-time, minimize logistics of sample permits/shipping, contribute to in-country capacity-building, and (our focus here) facilitate cross-site collaboration through shared methods and a shared laboratory. Here we provide proof-of-concept that an on-site hormone laboratory (the Taboga Field Laboratory, located in the Taboga Forest Reserve, Costa Rica) can successfully run endocrine analyses in a remote location. Using fecal samples from wild white-faced capuchins (Cebus imitator) from three Costa Rican forests, we validate the extraction and analysis of four steroid hormones (glucocorticoids, testosterone, estradiol, progesterone) across six assays (DetectX® and ISWE, all from Arbor Assays). Additionally, as the first collaboration across three long-term, wild capuchin field sites (Lomas Barbudal, Santa Rosa, Taboga) involving local Costa Rican collaborators, this laboratory can serve as a future hub for collaborative exchange.

The Goldilocks effect: female geladas in mid-sized groups have higher fitness.

The cost-benefit ratio of group living is thought to vary with group size: individuals in 'optimally sized' groups should have higher fitness than individuals in groups that are either too large or too small. However, the relationship between group size and individual fitness has been difficult to establish for long-lived species where the number of groups studied is typically quite low. Here, we present evidence for optimal group size that maximizes female fitness in a population of geladas (Theropithecus gelada). Drawing on 14 years of demographic data, we found that females in small groups experienced the highest death rates, while females in mid-sized groups exhibited the highest reproductive performance. This group size effect on female reproductive performance was largely explained by variation in infant mortality (and, in particular, by infanticide from immigrant males) but not by variation in reproductive rates. Taken together, females in mid-sized groups are projected to attain optimal fitness due to conspecific infanticide and, potentially, predation. Our findings provide insight into how and why group size shapes fitness in long-lived species.

The structural and motivational role of the unique lip-flip movement in the gelada (Theropithecus gelada) facial display repertoire.

OBJECTIVES: Human language represents an extreme form of communicative complexity. Primate facial display complexity, which depends upon facial mobility, can be used as a model for the study of the evolution of communicative complexity. The gelada (Theropithecus gelada) is the only primate that can produce a lip-flip eversion. This study investigates the role of the lip-flip relative to the bared-teeth display to understand its role in generating communicative complexity. MATERIALS AND METHODS: We reviewed videos of gelada social interactions. We utilized the facial action coding system (FACS) to define structural component action units (AUs) of each display. We inferred display motivation from the behaviors of the display sender. RESULTS: The lip-flip was used only in combination with the essential AUs of the bared-teeth display, serving as an optional structural element added to produce a structural variant. Both the bared-teeth display with and without a lip-flip occurred most frequently with nonaggressive, submissive behaviors. The lip-flip was more frequently preceded by approach than the bared-teeth display, especially in males. The lip-flip was also present in the majority of structurally blended facial displays though the motivation of the non-lip-flip parent display often dominated. DISCUSSION: The lip-flip may potentially function as an indicator of benign intent after an approach or as an intensifying component of nonaggressive intent. Adaptations to increase facial mobility in geladas via facilitating the lip-flip may promote increased communicative complexity through increased conspicuousness and motivational signaling specification or intensification.

High density of white-faced capuchins (Cebus capucinus) and habitat quality in the Taboga Forest of Costa Rica.

Across the globe, primates are threatened by human activities. This is especially true for species found in tropical dry forests, which remain largely unprotected. Our ability to predict primate abundance in the face of human activity depends on different species' sensitivities as well as on the characteristics of the forest itself. We studied plant and primate distribution and abundance in the Taboga Forest, a 516-ha tropical dry forest surrounded by agricultural fields in northwestern Costa Rica. We found that the density of white-faced capuchins (Cebus capucinus) at Taboga is 2-6 times higher than reported for other long-term white-faced capuchin sites. Using plant transects, we also found relatively high species richness, diversity, and equitability compared with other tropical dry forests. Edge transects (i.e., within 100 m from the forest boundary) differed from interior transects in two ways: (a) tree species associated with dry forest succession were well-established in the edge and (b) canopy cover in the edge was maintained year-round, while the interior forest was deciduous. Sighting rates for capuchins were higher near water sources but did not vary between the edge and interior forest. For comparison, we also found the same to be true for the only other primate in the Taboga Forest, mantled howler monkeys (Alouatta palliata). Year-round access to water might explain why some primate species can flourish even alongside anthropogenic disturbance. Forest fragments like Taboga may support high densities of some species because they provide a mosaic of habitats and key resources that buffer adverse ecological conditions.

Gelada vocal sequences follow Menzerath's linguistic law.

Identifying universal principles underpinning diverse natural systems is a key goal of the life sciences. A powerful approach in addressing this goal has been to test whether patterns consistent with linguistic laws are found in nonhuman animals. Menzerath's law is a linguistic law that states that, the larger the construct, the smaller the size of its constituents. Here, to our knowledge, we present the first evidence that Menzerath's law holds in the vocal communication of a nonhuman species. We show that, in vocal sequences of wild male geladas (Theropithecus gelada), construct size (sequence size in number of calls) is negatively correlated with constituent size (duration of calls). Call duration does not vary significantly with position in the sequence, but call sequence composition does change with sequence size and most call types are abbreviated in larger sequences. We also find that intercall intervals follow the same relationship with sequence size as do calls. Finally, we provide formal mathematical support for the idea that Menzerath's law reflects compression-the principle of minimizing the expected length of a code. Our findings suggest that a common principle underpins human and gelada vocal communication, highlighting the value of exploring the applicability of linguistic laws in vocal systems outside the realm of language.

Quantifying uncertainty due to fission-fusion dynamics as a component of social complexity.

Groups of animals (including humans) may show flexible grouping patterns, in which temporary aggregations or subgroups come together and split, changing composition over short temporal scales, (i.e. fission and fusion). A high degree of fission-fusion dynamics may constrain the regulation of social relationships, introducing uncertainty in interactions between group members. Here we use Shannon's entropy to quantify the predictability of subgroup composition for three species known to differ in the way their subgroups come together and split over time: spider monkeys (Ateles geoffroyi), chimpanzees (Pan troglodytes) and geladas (Theropithecus gelada). We formulate a random expectation of entropy that considers subgroup size variation and sample size, against which the observed entropy in subgroup composition can be compared. Using the theory of set partitioning, we also develop a method to estimate the number of subgroups that the group is likely to be divided into, based on the composition and size of single focal subgroups. Our results indicate that Shannon's entropy and the estimated number of subgroups present at a given time provide quantitative metrics of uncertainty in the social environment (within which social relationships must be regulated) for groups with different degrees of fission-fusion dynamics. These metrics also represent an indirect quantification of the cognitive challenges posed by socially dynamic environments. Overall, our novel methodological approach provides new insight for understanding the evolution of social complexity and the mechanisms to cope with the uncertainty that results from fission-fusion dynamics.

Alouatta pigra males ignore A. palliata loud calls: A case of failed rival recognition?

OBJECTIVES: When closely related species overlap geographically, selection may favor species-specific mate recognition traits to avoid hybridization costs. Conversely, the need to recognize potential same-sex rivals may select for lower specificity, creating the possibility that selection in one domain constrains evolution in the other. Despite a wealth of data on mate recognition, studies addressing rival recognition between hybridizing species are limited to a few bird species. Using naïve populations, we examine the extent to which failed rival recognition might have affected hybridization patterns when two species of howler monkeys (Alouatta pigra and A. palliata) first met after diverging in allopatry. METHODS: We simulated first contact between naïve subjects using playback experiments in allopatric populations of the two purebred species. Using linear mixed models, we compared their look, move, and vocal responses to conspecific and heterospecific loud calls. RESULTS: Although not different in overall response strength to playbacks, the two species differed in reaction to heterospecific callers. Male A. pigra ignored calls from male A. palliata, but the reverse was not true. DISCUSSION: Despite striking differences in vocalizations, A. palliata respond equally to calls from both species whereas A. pigra respond only to conspecifics. This apparent failure of A. pigra males to recognize interspecific rivals might have biased hybridization (F1 hybrids = male A. palliata x female A. pigra), a pattern previously hypothesized based on genetic analysis of hybrids. Given that A. pigra males could be losing reproductive opportunities to heterospecific males, our findings add to growing evidence of potential costs for overly specific species recognition.

The next step for stress research in primates: To identify relationships between glucocorticoid secretion and fitness.

Glucocorticoids are hormones that mediate the energetic demands that accompany environmental challenges. It is therefore not surprising that these metabolic hormones have come to dominate endocrine research on the health and fitness of wild populations. Yet, several problems have been identified in the vertebrate research that also apply to the non-human primate research. First, glucocorticoids should not be used as a proxy for fitness (unless a link has previously been established between glucocorticoids and fitness for a particular population). Second, stress research in behavioral ecology has been overly focused on "chronic stress" despite little evidence that chronic stress hampers fitness in wild animals. Third, research effort has been disproportionately focused on the causes of glucocorticoid variation rather than the fitness consequences. With these problems in mind, we have three objectives for this review. We describe the conceptual framework behind the "stress concept", emphasizing that high glucocorticoids do not necessarily indicate a stress response, and that a stress response does not necessarily indicate an animal is in poor health. Then, we conduct a comprehensive review of all studies on "stress" in wild primates, including any study that examined environmental factors, the stress response, and/or fitness (or proxies for fitness). Remarkably, not a single primate study establishes a connection between all three. Finally, we provide several recommendations for future research in the field of primate behavioral endocrinology, primarily the need to move beyond identifying the factors that cause glucocorticoid secretion to additionally focus on the relationship between glucocorticoids and fitness. We believe that this is an important next step for research on stress physiology in primates.

High mortality associated with tapeworm parasitism in geladas (Theropithecus gelada) in the Simien Mountains National Park, Ethiopia.

Despite increasing appreciation for parasitism as an important component of primate ecology and evolution, surprisingly few studies have demonstrated the costs of helminth parasitism in primates. Detecting parasite-related costs in primates is particularly difficult because it requires detailed, long-term data on individual host reproductive success, survival, and parasitism. The identification of the larval tapeworm Taenia serialis in geladas under intensive long-term study in the Ethiopian Highlands (Nguyen et al. [2015] American Journal of Primatology, 77:579-594; Schneider-Crease et al. [2013] Veterinary Parasitology 198:240-243) provides an opportunity to examine how an endemic parasite impacts host reproductive success and survival. We used survival analyses to assess the mortality risk associated with protuberant larval cysts characteristic of T. serialis using a decade of data from a gelada population in the Simien Mountains National Park (SMNP), Ethiopia. We demonstrated strikingly high mortality associated with T. serialis cysts in adult females, particularly for younger adults. The estimated effect of cysts on male mortality was similar, although the effect was not statistically significant, likely owing to the smaller sample size. Additionally, the offspring of mothers with cysts experienced increased mortality, which was driven almost entirely by maternal death. Mothers with cysts had such high mortality that they rarely completed an interbirth interval. Comparison with a study of this parasite in another gelada population on the Guassa Plateau (Nguyen et al. [2015] American Journal of Primatology, 77:579-594) revealed lower cyst prevalence in the SMNP and similar cyst-associated mortality. However, many more females with cysts completed interbirth intervals at Guassa than in the SMNP, suggesting that T. serialis cysts may kill hosts more rapidly in the SMNP. Our results point toward the underlying causes of individual and population-level heterogeneity in T. serialis-associated mortality as important areas for future research.

Growth trajectories in wild geladas (Theropithecus gelada).

Life history and socioecological factors have been linked to species-specific patterns of growth across female vertebrates. For example, greater maternal investment in offspring has been associated with more discrete periods of growth and reproduction. However, in primates it has been difficult to test such hypotheses because very few studies have obtained growth measurements from wild populations. Here we utilize a promising noninvasive photogrammetric method-parallel lasers-to examine shoulder-rump (SR) growth in a wild primate, the gelada (Theropithecus gelada, Simien Mountains National Park, Ethiopia). In this species, a graminivorous diet coupled with high extrinsic infant mortality risk suggests that maternal investment in neonates is low. Therefore, in contrast with other closely related papionins, we expected female geladas to exhibit less discrete periods of growth and reproduction. For both sexes, we compared size-for-age patterns (N = 154 females; N = 110 males) and changes in growth velocity relative to major life history milestones. Female geladas finished 88.5% of SR growth by first sexual swelling, and 97.2% by first reproduction, reaching adult body size by 7.72 years of age. Compared to closely related papionins, gelada females finished more growth by first reproduction, despite producing relatively small, and presumably "cheap," neonates. Male geladas finished 85.4% of growth at dispersal, and 96.0% at estimated first birth. Contrary to other polygynous primates, males are larger than females because they grow for a longer period of time (not because they grow faster), surpassing females around 6 years of age when female growth slows. Our results demonstrate that parallel lasers are an easy and promising new method that can be used to construct comprehensive life history perspectives that were once out of reach for wild populations. Am. J. Primatol. 78:707-719, 2016. © 2016 Wiley Periodicals, Inc.

Striking differences in the loud calls of howler monkey sister species (Alouatta pigra and A. palliata).

Comparing vocalizations across species is useful for understanding acoustic variation at mechanistic and evolutionary levels. Here, we take advantage of the divergent vocalizations of two closely related howler monkey species (Alouatta pigra and A. palliata) to better understand vocal evolution. In addition to comparing multiple acoustic and temporal features of roars and the calling bouts in which they are produced, we tested several predictions. First, A. pigra should have roars with lower fundamental frequency and lower formant dispersion because they are larger than A. palliata and have a larger hyoid apparatus. Second, A. pigra should have faster calling rates, longer roars, longer bouts, and exaggerated call features linked to vocal effort (e.g., nonlinear phenomena and emphasized frequencies) because they are the more aggressive species during intergroup encounters. We found significant interspecific differences supporting our predictions in every tested parameter of roars and bouts, except for roar duration and barking rate. Stepwise discriminant function analyses identified the best features for differentiating roars (acoustic features: formant dispersion followed by highest frequency; temporal features: longest syllable duration followed by number of syllables). Although resembling each other more than they resemble South American howler monkeys, our comparison revealed striking differences in the vocalizations of the two Mesoamerican species. While we cannot completely rule out the influence of body size or the environmental conditions in which the two species evolved, vocal differences were likely influenced by sexual selection. The exaggerated roars and intense calling patterns in A. pigra seem more suitable for intergroup competition, whereas A. palliata calls may be better suited for mate attraction and competition within groups. With interspecific acoustic differences quantified, we will now be able to examine how vocalizations contribute to the evolutionary dynamics of the A. palliata × A. pigra hybrid zone in southern Mexico. Am. J. Primatol. 78:755-766, 2016. © 2016 Wiley Periodicals, Inc.

The socio-genetics of a complex society: female gelada relatedness patterns mirror association patterns in a multilevel society.

Multilevel societies with fission-fusion dynamics--arguably the most complex animal societies--are defined by two or more nested levels of organization. The core of these societies are modular social units that regularly fission and fuse with one another. Despite convergent evolution in disparate taxa, we know strikingly little about how such societies form and how fitness benefits operate. Understanding the kinship structure of complex societies could inform us about the origins of the social structure as well as about the potential for individuals in these societies to accrue indirect fitness benefits. Here, we combined genetic and behavioural data on geladas (Theropithecus gelada), an Old World Monkey, to complete the most comprehensive socio-genetic analysis of a multilevel society to date. In geladas, individuals in the core social 'units', associate at different frequencies to form 'teams', 'bands' and, the largest aggregations, 'communities'. Units were composed of closely related females, and females remained with their close kin during permanent fissions of units. Interestingly, female-female relatedness also significantly predicted between-unit, between-team and between-band association patterns, while male-male relatedness did not. Thus, it is likely that the socio-genetic structure of gelada society results from females maintaining associations with their female relatives during successive unit fissions--possibly in an attempt to balance the direct and indirect fitness benefits of group living. Overall, the persistence of associations among related females across generations appears to drive the formation of higher levels of gelada society, suggesting that females seek kin for inclusive fitness benefits at multiple levels of gelada society.

Effect of ancestry on behavioral variation in two species of howler monkeys (Alouatta pigra and A. palliata) and their hybrids.

Social differences between primate species may result from both flexible responses to current conditions or fixed differences across taxa, yet we know little about the relative importance of these factors. Here, we take advantage of a naturally occurring hybrid zone in Tabasco, Mexico to characterize the variation in social structure among two endangered howler monkey species, Alouatta pigra and A. palliata, and their hybrids. Work in pure populations has suggested that A. pigra females maintain closer proximity, exhibit higher rates of affiliation, and lower rates of agonism than A. palliata females, but we do not know what accounts for this difference. Using identical data collection and analysis methods across three populations, we first seek to confirm previously reported interspecific differences in social structure across all sexes. We next examine: (1) how female social relationships changed with ancestry (by comparing pure and hybrid individuals); (2) how female social relationships changed with group size (A. pigra have smaller groups than A. palliata); and (3) whether female social relationships differed between two taxonomic groups within a single forest fragment (thus controlling for ecological variation). We confirmed previously described species differences, including closer proximity among females than among males in all populations. We also found that smaller groups maintained closer proximity. However, even after accounting for variation in group size, A. pigra females had closer proximity and more affiliation than A. palliata females. Furthermore, differences between pigra-like and palliata-like hybrids paralleled differences between pure populations and persisted even after controlling for ecological variation. Together, our results suggest that flexibility cannot account for all of the social differences between A. pigra and A. palliata and indicate an important genetic component in primate social behavior.

Social knowledge and signals in primates.

Primates are notable for having a rich and detailed understanding of their social environment and there has been great interest in the evolution and function of social knowledge in primates. Indeed, primates have been shown to have impressive understandings of not only other group members but also the complex relationships among them. To be useful, however, social knowledge requires memories from previous encounters and observations about individual traits that are stable. Here, we argue that social systems or traits that make social knowledge more costly or less accurate will favor signals that either supplement or replace social knowledge. Thus, the relationship between signals and social knowledge can be complementary or antagonistic depending on the type of signal. Our goal in this review is to elucidate the relationships between signals and social knowledge in primates. We categorize signals into three types, each with different relationships to social knowledge. (1) Identity signals directly facilitate social knowledge, (2) current-state signals supplement information gained through social knowledge, and (3) badges of status replace social knowledge. Primates rely extensively on identity information, but it remains to be determined to what extent this is based on receiver perception of individual variation or senders using identity signals. Primates frequently utilize current-state signals including signals of intent to augment their interactions with familiar individuals. Badges of status are rare in primates, and the cases where they are used point to a functional and evolutionary trade-off between badges of status and social knowledge. However, the nature of this relationship needs further exploration.

Information Ecology: an integrative framework for studying animal behavior.

Information is simultaneously a valuable resource for animals and a tractable variable for researchers. We propose the name Information Ecology to describe research focused on how individual animals use information to enhance fitness. An explicit focus on information in animal behavior is far from novel - we simply build on these ideas and promote a unified approach to how and why animals use information. The value of information to animals favors the theoretically rich adaptive approach of field-based research. Simultaneously, our ability to manipulate information lends itself to the strong methods of laboratory-based research. Information Ecology asks three questions: What information is available? How is it used (or not)? And, why is it used (or not)?

Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups.

By living in social groups with potential competitors, animals forgo monopolizing access to resources. Consequently, debate continues over how selection might favour sociality among competitors. For example, several models exist to account for the evolution of shared reproduction in groups. The 'concession model' hypothesizes that dominant reproducers benefit from the presence of subordinates, and hence tolerate some reproduction by subordinates. This mutual benefit to both dominants and subordinates may provide a foundation for the formation of social groups in which multiple members reproduce--a necessary step in the evolution of cooperation. To date, however, the concession model has received virtually no support in vertebrates. Instead, the vast majority of vertebrate data support 'limited control models', which posit that dominant reproducers are simply unable to prevent subordinates from reproducing. Here we present the most comprehensive evidence to date in support of the concession model in a vertebrate. We examined natural variation in the number of adult males in gelada (Theropithecus gelada) reproductive units to assess the extent of reproductive skew in multi-male units. Dominant ('leader') males in units that also had subordinate ('follower') males had a 30 per cent longer tenure than leaders in units that did not have followers, mainly because followers actively defended the group against potential immigrants. Follower males also obtained a small amount of reproduction in the unit, which may have functioned as a concession in return for defending the unit. These results suggest that dominants and subordinates may engage in mutually beneficial reproductive transactions, thus favouring male-male tolerance and cooperation.

Social drivers of maturation age in female geladas.

Female reproductive maturation is a critical life-history milestone, initiating an individual's reproductive career. Studies in social mammals have often focused on how variables related to nutrition influence maturation age in females. However, parallel investigations have identified conspicuous male-mediated effects in which female maturation is sensitive to the presence and relatedness of males. Here, we evaluated whether the more "classic" socioecological variables (i.e., maternal rank, group size) predict maturation age in wild geladas-a primate species with known male-mediated effects on maturation and a grassy diet that is not expected to generate intense female competition. Females delayed maturation in the presence of their fathers and quickly matured when unrelated, dominant males arrived. Controlling for these male effects, however, higher-ranking daughters matured at earlier ages than lower-ranking daughters, suggesting an effect of within-group contest competition. However, contrary to predictions related to within-group scramble competition, females matured earliest in larger groups. We attribute this result to either: 1) a shift to "faster" development in response to the high infant mortality risk posed by larger groups; or 2) accelerated maturation triggered by brief, unobserved male visits. While earlier ages at maturation were indeed associated with earlier ages at first birth, these benefits were occasionally offset by male takeovers, which can delay successful reproduction via spontaneous abortion. In sum, rank-related effects on reproduction can still occur even when socioecological theory would predict otherwise, and males (and the risks they pose) may prompt female maturation even outside of successful takeovers.