German Primate Center
  • Göttingen, Lower Saxony, Germany
Recent publications
In recent years, the utility and efficiency of automated procedures for cognitive assessment in psychology and neuroscience have been demonstrated in non-human primates (NHP). This approach mimics conventional shaping principles of breaking down a final desired behavior into smaller components that can be trained in a staircase manner. When combined with home-cage-based approaches, this could lead to a reduction in human workload, enhancement in data quality, and improvement in animal welfare. However, to our knowledge, there are no reported attempts to develop automated training and testing protocols for long-tailed macaques (Macaca fascicularis), a ubiquitous NHP model in neuroscience and pharmaceutical research. In the current work, we present the results from 6 long-tailed macaques that were trained using an automated unsupervised training (AUT) protocol for introducing the animals to the basics of a two-alternative choice (2 AC) task where they had to discriminate a conspecific vocalization from a pure tone relying on images presented on a touchscreen to report their response. We found that animals (1) consistently engaged with the device across several months; (2) interacted in bouts of high engagement; (3) alternated peacefully to interact with the device; and (4) smoothly ascended from step to step in the visually guided section of the procedure, in line with previous results from other NHPs. However, we also found (5) that animals' performance remained at chance level as soon as the acoustically guided steps were reached; and (6) that the engagement level decreased significantly with decreasing performance during the transition from visual to acoustic-guided sections. We conclude that with an autonomous approach, it is possible to train long-tailed macaques in their social group using computer vision techniques and without dietary restriction to solve a visually guided discrimination task but not an acoustically guided task. We provide suggestions on what future attempts could take into consideration to instruct acoustically guided discrimination tasks successfully.
The development of the unique, hierarchical and endless combinatorial capacity in human language requires neural maturation and learning through childhood. Compared with most non‐human primates, where combinatorial capacity seems limited, chimpanzees present a complex vocal system comprising hundreds of vocal sequences. We investigated how such a complex vocal system develops and the processes involved. We recorded 10,929 vocal utterances of 98 wild chimpanzees aged 0 to 55 years, from Taï National Park, Ivory Coast. We developed customized Generalized non‐Linear Models to estimate the ontogenetic trajectory of four structural components of vocal complexity: utterance length, diversity, probability of panting (requiring phonation across inhalation and exhalation), and probability of producing two adjacent panted units. We found chimpanzees need 10 years to reach adult‐levels of vocal complexity. In three variables, the steepest increase coincided with the age of first non‐kin social interactions (2‐5 years), and plateaued in sub‐adults (8‐10 years), as individuals integrate into adult social life. Producing two adjacent panted units may require more neuromuscular coordination of the articulators, as its emergence and steepest increase appear later in development. These results suggest prolonged maturational processes beyond those hitherto thought likely in species that do not learn their vocal repertoire. Our results suggest that multifaceted ontogenetic processes drive increases in vocal structural complexity in chimpanzees, particularly increases in social complexity and neuro‐muscular maturation. As humans live in a complex social world, empirical support for the “social complexity hypothesis” may have relevance for theories of language evolution. This article is protected by copyright. All rights reserved
Previous research on adaptive NK cells in rhesus macaques suffered from the lack of specific antibodies to differentiate between inhibitory CD94/NKG2A and stimulatory CD94/NKG2C heterodimeric receptors. Recently we reported an expansion of NKG2C receptor-encoding genes in rhesus macaques, but their expression and functional role on primary NK cells remained unknown due to this deficit. Thus, we established monoclonal antibodies 4A8 and 7B1 which show identical specificities and bind to both NKG2C-1 and NKG2C-2 but neither react with NKG2C-3 nor NKG2A on transfected cells. Using a combination of 4A8 and Z199 antibodies in multicolor flow cytometry we detected broad expression (4-73%) of NKG2C-1 and/or NKG2C-2 (NKG2C-1/2) on primary NK cells in rhesus macaques from our breeding colony. Stratifying our data to CMV-positive and CMV-negative animals, we noticed a higher proportion (23-73%) of primary NK cells expressing NKG2C-1/2 in CMV+ as compared to CMV-macaques (4-5%). These NKG2C-1/2-positive NK cells in CMV+ macaques are characterized by lower expression of IL12RB2, ZBTB16, SH2D1B, but not FCER1G, as well as high expression of IFNG, indicating that antibody 4A8 detects CMV-associated adaptive NK cells. Single cell RNA seq data of 4A8-positive NK cells from a rhCMV-positive macaque demonstrated that a high proportion of these adaptive NK cells transcribe in addition to NKG2C-1 and NKG2C-2 also NKG2C-3, but interestingly NKG2A as well. Remarkably, in comparison to NKG2A, NKG2C-1 and in particular NKG2C-2 bind Mamu-E with higher avidity. Primary NK cells exposed to Mamu-E-expressing target cells displayed strong degranulation as well as IFN-gamma expression of 4A8+ adaptive NK cells from rhCMV+ animals. Thus, despite co-expression of inhibitory and stimulatory CD94/NKG2 receptors the higher number of different stimulatory NKG2C receptors and their higher binding avidity to Mamu-E outreach inhibitory signaling via NKG2A. These data Frontiers in Immunology demonstrate the evolutionary conservation of the CMV-driven development of NKG2C-positive adaptive NK cells with particular molecular signatures in primates and with changes in gene copy numbers and ligand-binding strength of NKG2C isotypes. Thus, rhesus macaques represent a suitable and valuable nonhuman primate animal model to study the CMV-NKG2C liaison in vivo.
SARS-CoV-2 variants accumulating immune escape mutations provide a significant risk to vaccine-induced protection against infection. The novel variant of concern (VoC) Omicron BA.1 and its sub-lineages have the largest number of amino acid alterations in its Spike protein to date. Thus, they may efficiently escape recognition by neutralizing antibodies, allowing breakthrough infections in convalescent and vaccinated individuals in particular in those who have only received a primary immunization scheme. We analyzed neutralization activity of sera from individuals after vaccination with all mRNA-, vector- or heterologous immunization schemes currently available in Europe by in vitro neutralization assay at peak response towards SARS-CoV-2 B.1, Omicron sub-lineages BA.1, BA.2, BA.2.12.1, BA.3, BA.4/5, Beta and Delta pseudotypes and also provide longitudinal follow-up data from BNT162b2 vaccinees. All vaccines apart from Ad26.CoV2.S showed high levels of responder rates (96–100%) towards the SARS-CoV-2 B.1 isolate, and minor to moderate reductions in neutralizing Beta and Delta VoC pseudotypes. The novel Omicron variant and its sub-lineages had the biggest impact, both in terms of response rates and neutralization titers. Only mRNA-1273 showed a 100% response rate to Omicron BA.1 and induced the highest level of neutralizing antibody titers, followed by heterologous prime-boost approaches. Homologous BNT162b2 vaccination, vector-based AZD1222 and Ad26.CoV2.S performed less well with peak responder rates of 48%, 56% and 9%, respectively. However, Omicron responder rates in BNT162b2 recipients were maintained in our six month longitudinal follow-up indicating that individuals with cross-protection against Omicron maintain it over time. Overall, our data strongly argue for booster doses in individuals who were previously vaccinated with BNT162b2, or a vector-based primary immunization scheme.
Behavioral discrimination of kin is a key process structuring social relationships in animals. In this study, we provide evidence for discrimination towards non-kin by third-parties through a mechanism of phenotype matching. In mandrills, we recently demonstrated increased facial resemblance among paternally related juvenile and adult females indicating adaptive opportunities for paternal kin recognition. Here, we hypothesize that mandrill mothers use offspring’s facial resemblance with other infants to guide offspring’s social opportunities towards similar-looking ones. Using deep learning for face recognition in 80 wild mandrill infants, we first show that infants sired by the same father resemble each other the most, independently of their age, sex or maternal origin, extending previous results to the youngest age class. Using long-term behavioral observations on association patterns, and controlling for matrilineal origin, maternal relatedness and infant age and sex, we then show, as predicted, that mothers are spatially closer to infants that resemble their own offspring more, and that this maternal behavior leads to similar-looking infants being spatially associated. We then discuss the different scenarios explaining this result, arguing that an adaptive maternal behavior is a likely explanation. In support of this mechanism and using theoretical modeling, we finally describe a plausible evolutionary process whereby mothers gain fitness benefits by promoting nepotism among paternally related infants. This mechanism, that we call ‘second-order kin selection’, may extend beyond mother-infant interactions and has the potential to explain cooperative behaviors among non-kin in other social species, including humans.
Recently, a recombinant SARS-CoV-2 lineage, XD, emerged that harbors a spike gene that is largely derived from the Omicron variant BA.1 in the genetic background of the Delta variant. This finding raised concerns that the recombinant virus might exhibit altered biological properties as compared to the parental viruses and might pose an elevated threat to human health. Here, using pseudotyped particles, we show that ACE2 binding and cell tropism of XD mimics that of BA.1. Further, XD and BA.1 displayed comparable sensitivity to neutralization by antibodies induced upon vaccination with BNT162b2/Comirnaty (BNT) or BNT vaccination followed by breakthrough infection. Our findings reveal important biological commonalities between XD and Omicron BA.1 host cell entry and its inhibition by antibodies.
The spike (S) protein of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) facilitates viral entry into host cells and is the key target for neutralizing antibodies. The SARS-CoV-2 lineage B.1.620 carries fifteen mutations in the S protein and is spread in Africa, the US and Europe, while lineage R.1 harbors four mutations in S and infections were observed in several countries, particularly Japan and the US. However, the impact of the mutations in B.1.620 and R.1 S proteins on antibody-mediated neutralization and host cell entry are largely unknown. Here, we report that these mutations are compatible with robust ACE2 binding and entry into cell lines, and they markedly reduce neutralization by vaccine-induced antibodies. Our results reveal evasion of neutralizing antibodies by B.1.620 and R.1, which might have contributed to the spread of these lineages.
Owl monkeys (genus Aotus), or “night monkeys” are platyrrhine primates in the Aotidae family. Early taxonomy only recognized one species, Aotus trivirgatus, until 1983, when Hershkovitz proposed nine unique species designations, classified into red-necked and gray-necked species groups based predominately on pelage coloration. Recent studies questioned this conventional separation of the genus and proposed designations based on the geographical location of wild populations. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. A scaffold-level genome assembly for one Aotus species, Aotus nancymaae [Anan_2.0], facilitated large-scale ascertainment of nearly 2000 young lineage-specific Alu insertions. This study provides candidate oligonucleotides for locus-specific PCR assays for over 1350 of these elements. For 314 Alu elements across four taxa with multiple specimens, PCR analyses identified 159 insertion polymorphisms, including 21 grouping A. nancymaae and Aotus azarae (red-necked species) as sister taxa, with Aotus vociferans and A. trivirgatus (gray-necked) being more basal. DNA sequencing identified five novel Alu elements from three different taxa. The Alu datasets reported in this study will assist in species identification and provide a valuable resource for Aotus phylogenetics, population genetics and conservation strategies when applied to wild populations.
Androgens offer a window into the timing of important male life history events such as maturation. However, when males are the dispersing sex, piecing together normative androgen profiles across development is challenging because dispersing males are difficult to track. Here, we examined the conditions that may be associated with male androgen status (via fecal androgen metabolites, fAMs) and age at dispersal in wild male geladas (Theropithecus gelada). Gelada male life histories are highly variable — dispersal may occur before sexual maturation, dispersal itself can be immediate or drawn out, and, due to their multi-leveled society, social conditions affecting dispersal can vary for juveniles living in different reproductive units within the same band. Using longitudinal data from known natal males, we examined how androgen levels and age at dispersal were associated with: (1) access to maternal resources (i.e., maternal rank, birth of a younger sibling, experiencing maternal loss), and (2) access to male peers (i.e., number of similar-aged males in their unit). We found that androgens were significantly lower in males with high-ranking mothers (in males >2.5 years of age; infant androgens were unrelated) and that having more male peers in their social group and larger groups overall predicted an earlier age at dispersal. Moreover, dispersal in geladas was not preceded or followed by a surge in androgen levels. Taken together, results suggest that social environments can cause individual variation in androgens and dispersal age. Whether this variation leads to differences in male fitness in later life remains to be determined.
Inhibitory control requires an individual to suppress impulsive actions in favour of more appropriate behaviours to gain a delayed reward. It plays an important role in activities such as foraging and initiating mating, but high within-species variation suggests that some individuals have greater inhibitory control than others. A standard index of inhibitory control used in many taxa is measuring how long an animal persists in trying to move itself or an appendage (e.g. its hand) through a transparent barrier to reach a reward. Although recent nonhuman studies have investigated how different factors are associated with variation in inhibitory control, these studies have rarely considered how these factors interact. Here we investigated how sex, age, personality (boldness) and the type of reward stimulus interact to predict the degree of motor inhibitory control in eastern mosquitofish, Gambusia holbrooki. We measured inhibitory control using a standard detour assay, ‘boldness’ (time to emergence in a novel environment), and the rate of learning. There were three different reward stimuli: a shoal of females, a shoal of males or a mixed-sex shoal. Individuals were tested in four consecutive trials, always with the same reward type, to quantify short-term learning. These measures were repeated at 7, 14 and 21 weeks after maturation to examine the effect of age. Females had significantly greater inhibitory control than males. Regardless of sex, older fish had significantly greater inhibitory control than younger fish, and boldness predicted learning ability. The type of reward stimuli had no sex-specific effect on inhibitory control. We discuss the biological significance of these sources of variation in inhibitory control, and the importance of accounting for them in studies examining individual differences in cognitive abilities.
Recent progress in quantitative susceptibility mapping (QSM) has enabled the accurate delineation of submillimeter-scale subcortical brain structures in humans. However, the simultaneous visualization of cortical, subcortical, and white matter structure remains challenging, utilizing QSM data solely. Here we present TQ-SILiCON, a fusion method that enhances the contrast of cortex and subcortical structures and provides an excellent white matter delineation by combining QSM and conventional T1-weighted (T1w) images. In this study, we first applied QSM in the macaque monkey to map iron-rich subcortical structures. Implementing the same QSM acquisition and analysis methods allowed a similar accurate delineation of subcortical structures in humans. However, the QSM contrast of white and cortical gray matter was not sufficient for appropriate segmentation. Applying automatic brain tissue segmentation to TQ-SILiCON images of the macaque improved the classification of subcortical brain structures as compared to the single T1 contrast by maintaining an excellent white to cortical gray matter contrast. Furthermore, we validated our dual-contrast fusion approach in humans and similarly demonstrated improvements in automated segmentation of the cortex and subcortical structures. We believe the proposed contrast will facilitate translational studies in nonhuman primates to investigate the pathophysiology of neurodegenerative diseases that affect subcortical structures such as the basal ganglia in humans.
African wolves (Canis lupaster) and Ethiopian wolves (C. simensis) occur often sympatrically across habitats in the Ethiopian Highlands, with recent studies finding evidence for interspecific competition. However, unlike the well-studied Ethiopian wolf, comparatively little is known about the ecology of the African wolf in the Ethiopian Highlands. To address this empirical gap, we collected data on home range size, habitat use, and activity patterns of radio-collared African wolves at the Guassa Menz Community Conservation Area (GCCA) and Borena Saynt Worehimenu National Park (BSNP). We followed the African wolves (5 in GCCA, 6 in BSNP) for 16 months and had 659 ± 83 encounters with each individual. The mean 95% kernel density estimate home range size of African wolves was higher in BSNP (4.5 ± 1.5 km²) than at GCCA (2.2 ± 0.7 km²). In 55% (n=3,934) of the encounters the wolves were found to be solitary, whereas in other encounters we found them in groups of two to seven. At both sites, the African wolves were more often found in areas close to human settlements than in more intact habitat, and they were mainly active at dawn and dusk. These results show flexibility in African wolf socioecology in response to habitat fragmentation and anthropogenic disturbance. We recommend further studies on major causes of spatial and temporal niche partitioning of Ethiopian wolves and African wolves in the Ethiopian Highlands.
Converging lines of inquiry from across the social and biological sciences target the adult sex ratio (ASR; the proportion of males in the adult population) as a fundamental population-level determinant of behavior. The ASR, which indicates the relative number of potential mates to competitors in a population, frames the selective arena for competition, mate choice, and social interactions. Here we review a growing literature, focusing on methodological developments that sharpen knowledge of the demographic variables underlying ASR variation, experiments that enhance understanding of the consequences of ASR imbalance across societies, and phylogenetic analyses that provide novel insights into social evolution. We additionally highlight areas where research advances are expected to make accelerating contributions across the social sciences, evolutionary biology, and biodiversity conservation. A detailed Review across animal and human societies provides insight on the causes and consequences of adult sex ratio skew.
Purpose: To develop a free-breathing myocardial T 1 $$ {\mathrm{T}}_1 $$ mapping technique using inversion-recovery (IR) radial fast low-angle shot (FLASH) and calibrationless motion-resolved model-based reconstruction. Methods: Free-running (free-breathing, retrospective cardiac gating) IR radial FLASH is used for data acquisition at 3T. First, to reduce the waiting time between inversions, an analytical formula is derived that takes the incomplete T 1 $$ {\mathrm{T}}_1 $$ recovery into account for an accurate T 1 $$ {\mathrm{T}}_1 $$ calculation. Second, the respiratory motion signal is estimated from the k-space center of the contrast varying acquisition using an adapted singular spectrum analysis (SSA-FARY) technique. Third, a motion-resolved model-based reconstruction is used to estimate both parameter and coil sensitivity maps directly from the sorted k-space data. Thus, spatiotemporal total variation, in addition to the spatial sparsity constraints, can be directly applied to the parameter maps. Validations are performed on an experimental phantom, 11 human subjects, and a young landrace pig with myocardial infarction. Results: In comparison to an IR spin-echo reference, phantom results confirm good T 1 $$ {\mathrm{T}}_1 $$ accuracy, when reducing the waiting time from 5 s to 1 s using the new correction. The motion-resolved model-based reconstruction further improves T 1 $$ {\mathrm{T}}_1 $$ precision compared to the spatial regularization-only reconstruction. Aside from showing that a reliable respiratory motion signal can be estimated using modified SSA-FARY, in vivo studies demonstrate that dynamic myocardial T 1 $$ {\mathrm{T}}_1 $$ maps can be obtained within 2 min with good precision and repeatability. Conclusion: Motion-resolved myocardial T 1 $$ {\mathrm{T}}_1 $$ mapping during free-breathing with good accuracy, precision and repeatability can be achieved by combining inversion-recovery radial FLASH, self-gating and a calibrationless motion-resolved model-based reconstruction.
Recognizing emotions is an essential ability for successful interpersonal interaction. Prior research indicates some links between the endocrine system and emotion recognition ability, but only a few studies focused on within-subject differences across distinct ovulatory cycle phases and this ability. These studies have demonstrated mixed results that might be potentially due to heterogeneity in experimental tasks, methodologies, and lacking ecological validity. In the current study, we investigated associations between within-subject differences in ovarian hormones levels and emotion recognition from auditory, visual, and audiovisual modalities in N = 131 naturally cycling participants across the late follicular and mid-luteal phase of the ovulatory cycle. We applied a within-subject design with sessions in the late follicular and mid-luteal cycle phase, and also assessed salivary progesterone and estradiol in these sessions. Our findings did not reveal any significant difference in emotion recognition ability across two cycle phases. Thus, they emphasize the necessity of employing large-scale replication studies with well-established study designs along with proper statistical analyses. Moreover, our findings indicate that the potential link between ovulatory cycle phases (late follicular and mid-luteal) and emotion recognition ability might have been overestimated in previous studies, and may contribute to theoretical and practical implications of socio-cognitive neuroendocrinology.
Mutations in spike (S) protein epitopes allow SARS-CoV-2 variants to evade antibody responses induced by infection and/or vaccination. In contrast, glycosylation sites in the S protein are conserved across SARS-CoV-2 variants, making glycans a potential robust target for developing antivirals. However, this target has not been adequately exploited for SARS-CoV-2, mostly due to intrinsically weak monovalent protein-glycan inter-actions. We hypothesize that polyvalent nano-lectins with flexibly linked carbohydrate-recognition-domains (CRDs) can adjust their relative positions and bind multivalently to S protein glycans, potentially exerting potent antiviral activity. Herein, we displayed the CRDs of DC-SIGN, a dendritic cell lectin known to bind to diverse viruses, polyvalently onto 13 nm gold nanoparticles (named as G13-CRD). G13-CRD bound strongly and specifically to target glycan-coated quantum dots with sub-nM Kd. Moreover, G13-CRD neutralized particles pseudo-typed with the S proteins of Wuhan Hu-1, B1, Delta variant and Omicron subvariant BA.1 with low nM EC50. In contrast, natural tetrameric DC-SIGN and its G13 conjugate were ineffective. Further, G13-CRD potently and completely inhibited authentic SARS-CoV-2 Wuhan Hu-1 and BA.1, with <10 pM and <10 nM EC50, respectively. These results identify G13-CRD as a polyvalent nano-lectin with broad activity against SARS-CoV-2 variants that merits further exploration as a novel approach to antiviral therapy.
In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.
Saguinus mystax (Spix, 1823), a callitrichid (tamarin and marmoset family) commonly called the mustached tamarin, is 1 of 12 species in the genus Saguinus. In this large callitrichid (450–650 g), females are slightly heavier than males. It occurs in Brazil and Peru, south of Rio Amazonas from Río Ucayali in the west to Rio Purus in the east, in primary and secondary tierra firma rainforests. The diet consists of fruit pulp, insects, gums, nectar, and small vertebrates. It lives in groups of 3–10 individuals with a male-biased adult sex ratio and has a cooperative breeding system. In areas of sympatry, S. mystax forms mixed-species groups with saddle-back tamarins, Leontocebus. Although captured for the pet trade and sporadically hunted, it is considered “Least Concern” (LC) by the International Union for Conservation of Nature.
Nose picking (rhinotillexis) is a common behaviour in humans which remains, however, poorly studied. Several species of primates are known to pick their nose and ingest the nasal mucus suggesting that this behaviour may actually be beneficial and showing it is not restricted to humans. Here, we review relevant literature and online sources, and document the species of primates observed to pick their nose. We also present the first occurrence of this behaviour in a species of strepsirrhine primate (lemurs and relatives) with a unique video showing an aye‐aye picking its nose. While doing so this animal inserts the entire length of its extra‐long, skinny and highly mobile middle finger into the nasal passages and then licks the nasal mucus collected. We further investigate the internal anatomy of the nasal cavity of the aye‐aye in order to understand how it can introduce its entire finger in its nasal cavity and discover that the finger likely descends into the pharynx. We show that this behaviour is present in at least 12 species of primates, most of them also showing great manipulative/tool use skills and may have some associated benefits that need to be further investigated. Further comparative studies examining nose picking and mucophagy in other primate species and vertebrates in general may shed additional light on its evolution and possible functional role. We review and document nose picking and mucophagy in primates and present the first occurrence of this behaviour in a strepsirrhine primate with a unique video showing an aye‐aye picking its nose. We found that at least 12 species of primates pick their nose and ingest mucus, most of which also demonstrate high levels of manipulation skills and tool use. Further comparative studies of nose‐picking and mucophagy in other primates and in vertebrates more generally could shed further light on its evolution and possible functional role.
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168 members
Michael Winkler
  • Infection Biology Unit
Stefan Pöhlmann
  • Infection Biology Unit
Julia Fischer
  • Cognitive Ethology Laboratory
Hans Scherberger
  • Neurobiology Research Group
Stoyan G Petkov
  • Degenerative Diseases
Kellnerweg 4, 37077, Göttingen, Lower Saxony, Germany