Publications by authors named "Erik Willems"

59 Publications

Cooperative partner choice in multi-level male dolphin alliances.

Sci Rep 2021 Mar 25;11(1):6901. Epub 2021 Mar 25.

Evolutionary Genetics Group, Department of Anthropology, University of Zurich, 8057, Zurich, Switzerland.

Investigations into cooperative partner choice should consider both potential and realised partners, allowing for the comparison of traits across all those available. Male bottlenose dolphins form persisting multi-level alliances. Second-order alliances of 4-14 males are the core social unit, within which 2-3 males form first-order alliances to sequester females during consortships. We compared social bond strength, relatedness and age similarity of potential and realised partners of individual males in two age periods: (i) adolescence, when second-order alliances are formed from all available associates, and (ii) adulthood, when first-order allies are selected from within second-order alliances. Social bond strength during adolescence predicted second-order alliance membership in adulthood. Moreover, males preferred same-aged or older males as second-order allies. Within second-order alliances, non-mating season social bond strength predicted first-order partner preferences during mating season consortships. Relatedness did not influence partner choice on either alliance level. There is thus a striking resemblance between male dolphins, chimpanzees and humans, where closely bonded non-relatives engage in higher-level, polyadic cooperative acts. To that end, our study extends the scope of taxa in which social bonds rather than kinship explain cooperation, providing the first evidence that such traits might have evolved independently in marine and terrestrial realms.
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http://dx.doi.org/10.1038/s41598-021-85583-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7994371PMC
March 2021

The cost of associating with males for Bornean and Sumatran female orangutans: a hidden form of sexual conflict?

Behav Ecol Sociobiol 2021 30;75(1). Epub 2020 Dec 30.

Department of Anthropology, University of Zurich, Zurich, Switzerland.

Abstract: Sexual coercion, in the form of forced copulations, is relatively frequently observed in orangutans and generally attributed to their semi-solitary lifestyle. High ecological costs of association for females may be responsible for this lifestyle and may have prevented the evolution of morphological fertility indicators (e.g., sexual swellings), which would attract (male) associates. Therefore, sexual conflict may arise not only about mating per se but also about associations, because males may benefit from associations with females to monitor their reproductive state and attempt to monopolize their sexual activities. Here, we evaluate association patterns and costs for females when associating with both males and females of two different orangutan species at two study sites: Suaq, Sumatra (), and Tuanan, Borneo (). Female association frequency with both males and females was higher in the Sumatran population, living in more productive habitat. Accordingly, we found that the cost of association, in terms of reduced feeding to moving ratio and increased time being active, is higher in the less sociable Bornean population. Males generally initiated and maintained such costly associations with females, and prolonged associations with males led to increased female fecal cortisol metabolite (FCM) levels at Tuanan, the Bornean population. We conclude that male-maintained associations are an expression of sexual conflict in orangutans, at least at Tuanan. For females, this cost of association may be responsible for the lack of sexual signaling, while needing to confuse paternity.

Significance Statement: Socioecological theory predicts a trade-off between the benefits of sociality and the ecological costs of increased feeding competition. Orangutans' semi-solitary lifestyle has been attributed to the combination of high association costs and low predation risk. Previous work revealed a positive correlation between association frequencies and habitat productivity, but did not measure the costs of association. In this comparative study, we show that females likely incur costs from involuntary, male-maintained associations, especially when they last for several days and particularly in the population characterized by lower association frequencies. Association maintenance therefore qualifies as another expression of sexual conflict in orangutans, and especially prolonged, male-maintained associations may qualify as an indirect form of sexual coercion.

Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-020-02948-4.
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http://dx.doi.org/10.1007/s00265-020-02948-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7773621PMC
December 2020

Controls the Maturation of Dendrites, Synaptic Function, and Network Activity in Developing Human Neurons.

J Neurosci 2020 10 4;40(41):7980-7994. Epub 2020 Sep 4.

Department of Neuroscience, Scripps Research, Jupiter, Florida 33458

is a major genetic risk factor for global developmental delay, autism spectrum disorder, and epileptic encephalopathy. loss-of-function variants in this gene cause a neurodevelopmental disorder defined by cognitive impairment, social-communication disorder, and early-onset seizures. Cell biological studies in mouse and rat neurons have shown that regulates developing excitatory synapse structure and function, with loss-of-function variants driving formation of larger dendritic spines and stronger glutamatergic transmission. However, studies to date have been limited to mouse and rat neurons. Therefore, it remains unknown how loss of function impacts the development and function of human neurons. To address this, we used CRISPR/Cas9 technology to ablate protein expression in neurons derived from a commercially available induced pluripotent stem cell line (hiPSC) obtained from a human female donor. Reducing SynGAP protein expression in developing hiPSC-derived neurons enhanced dendritic morphogenesis, leading to larger neurons compared with those derived from isogenic controls. Consistent with larger dendritic fields, we also observed a greater number of morphologically defined excitatory synapses in cultures containing these neurons. Moreover, neurons with reduced SynGAP protein had stronger excitatory synapses and expressed synaptic activity earlier in development. Finally, distributed network spiking activity appeared earlier, was substantially elevated, and exhibited greater bursting behavior in null neurons. We conclude that regulates the postmitotic maturation of human neurons made from hiPSCs, which influences how activity develops within nascent neural networks. Alterations to this fundamental neurodevelopmental process may contribute to the etiology of -related disorders. is a major genetic risk factor for global developmental delay, autism spectrum disorder, and epileptic encephalopathy. While this gene is well studied in rodent neurons, its function in human neurons remains unknown. We used CRISPR/Cas9 technology to disrupt protein expression in neurons derived from an induced pluripotent stem cell line. We found that induced neurons lacking SynGAP expression exhibited accelerated dendritic morphogenesis, increased accumulation of postsynaptic markers, early expression of synapse activity, enhanced excitatory synaptic strength, and early onset of neural network activity. We conclude that regulates the postmitotic differentiation rate of developing human neurons and disrupting this process impacts the function of nascent neural networks. These altered developmental processes may contribute to the etiology of disorders.
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http://dx.doi.org/10.1523/JNEUROSCI.1367-20.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7548701PMC
October 2020

Affiliation history and age similarity predict alliance formation in adult male bottlenose dolphins.

Behav Ecol 2020 Mar-Apr;31(2):361-370. Epub 2019 Nov 28.

Department of Anthropology, Evolutionary Genetics Group, University of Zurich, Zurich, Switzerland.

Male alliances are an intriguing phenomenon in the context of reproduction since, in most taxa, males compete over an indivisible resource, female fertilization. Adult male bottlenose dolphins () in Shark Bay, Western Australia, form long-term, multilevel alliances to sequester estrus females. These alliances are therefore critical to male reproductive success. Yet, the long-term processes leading to the formation of such complex social bonds are still poorly understood. To identify the criteria by which male dolphins form social bonds with other males, we adopted a long-term approach by investigating the ontogeny of alliance formation. We followed the individual careers of 59 males for 14 years while they transitioned from adolescence (8-14 years of age) to adulthood (15-21 years old). Analyzing their genetic relationships and social associations in both age groups, we found that the vast majority of social bonds present in adolescence persisted through time. Male associations in early life predict alliance partners as adults. Kinship patterns explained associations during adolescence but not during adulthood. Instead, adult males associated with males of similar age. Our findings suggest that social bonds among peers, rather than kinship, play a central role in the development of adult male polyadic cooperation in dolphins.
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http://dx.doi.org/10.1093/beheco/arz195DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7083095PMC
November 2019

Extract WS®1442 Stimulates Cardiomyogenesis and Angiogenesis From Stem Cells: A Possible New Pharmacology for Hawthorn?

Front Pharmacol 2019 27;10:1357. Epub 2019 Nov 27.

Department of Chemistry and Chemical Biology, Technical University of Dortmund, Dortmund, Germany.

Extracts from the leaves and flowers of spp. (i.e., hawthorn species) have been traditionally used with documented preclinical and clinical activities in cardiovascular medicine. Based on reported positive effects on heart muscle after ischemic injury and the overall cardioprotective profile, the present study addressed potential contributions of extracts to cardiopoietic differentiation from stem cells. The quantified extract WS1442 stimulated cardiomyogenesis from murine and human embryonic stem cells (ESCs). Mechanistically, this effect was found to be induced by promoting differentiation of cardiovascular progenitor cell populations but not by proliferation. Bioassay-guided fractionation, phytochemical and analytical profiling suggested high-molecular weight ingredients as the active principle with at least part of the activity due to oligomeric procyanidines (OPCs) with a degree of polymerization between 3 and 6 (DP3-6). Transcriptome profiling in mESCs suggested two main, plausible mechanisms: These were early, stress-associated cellular events along with the modulation of distinct developmental pathways, including the upregulation of brain-derived neurotrophic factor (BDNF) and retinoic acid as well as the inhibition of transforming growth factor β/bone morphogenetic protein (TGFβ/BMP) and fibroblast growth factor (FGF) signaling. In addition, WS1442 stimulated angiogenesis in Sca-1 progenitor cells from adult mice hearts. These data provide evidence for a differentiation promoting activity of WS1442 on distinct cardiovascular stem/progenitor cells that could be valuable for therapeutic heart regeneration after myocardial infarction. However, the relevance of this new pharmacological activity of spp. remains to be investigated and active ingredients from bioactive fractions will have to be further characterized.
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http://dx.doi.org/10.3389/fphar.2019.01357DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6902660PMC
November 2019

Site-specific phosphorylation and caspase cleavage of GFAP are new markers of Alexander disease severity.

Elife 2019 11 4;8. Epub 2019 Nov 4.

Department of Cell Biology and Physiology, University of North Carolina, Chapel Hill, United States.

Alexander disease (AxD) is a fatal neurodegenerative disorder caused by mutations in glial fibrillary acidic protein (GFAP), which supports the structural integrity of astrocytes. Over 70 GFAP missense mutations cause AxD, but the mechanism linking different mutations to disease-relevant phenotypes remains unknown. We used AxD patient brain tissue and induced pluripotent stem cell (iPSC)-derived astrocytes to investigate the hypothesis that AxD-causing mutations perturb key post-translational modifications (PTMs) on GFAP. Our findings reveal selective phosphorylation of GFAP-Ser13 in patients who died young, independently of the mutation they carried. AxD iPSC-astrocytes accumulated pSer13-GFAP in cytoplasmic aggregates within deep nuclear invaginations, resembling the hallmark Rosenthal fibers observed in vivo. Ser13 phosphorylation facilitated GFAP aggregation and was associated with increased GFAP proteolysis by caspase-6. Furthermore, caspase-6 was selectively expressed in young AxD patients, and correlated with the presence of cleaved GFAP. We reveal a novel PTM signature linking different GFAP mutations in infantile AxD.
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http://dx.doi.org/10.7554/eLife.47789DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6927689PMC
November 2019

Are dialects socially learned in marmoset monkeys? Evidence from translocation experiments.

PLoS One 2019 23;14(10):e0222486. Epub 2019 Oct 23.

Department of Anthropology, University of Zurich, Winterthurerstrasse, Zürich, Switzerland.

The acoustic properties of vocalizations in common marmosets differ between populations. These differences may be the result of social vocal learning, but they can also result from environmental or genetic differences between populations. We performed translocation experiments to separately quantify the influence of a change in the physical environment (experiment 1), and a change in the social environment (experiment 2) on the acoustic properties of calls from individual captive common marmosets. If population differences were due to genetic differences, we expected no change in the vocalizations of the translocated marmosets. If differences were due to environmental factors, we expected vocalizations to permanently change contingent with environmental changes. If social learning was involved, we expected that the vocalizations of animals translocated to a new population with a different dialect would become more similar to the new population. In experiment 1, we translocated marmosets to a different physical environment without changing the social composition of the groups or their neighbours. Immediately after the translocation to the new facility, one out of three call types showed a significant change in call structure, but 5-6 weeks later, the calls were no longer different from before the translocation. Thus, the novel physical environment did not induce long lasting changes in the vocalizations of the marmosets. In experiment 2, we translocated marmosets to a new population with a different dialect. Importantly, our previous work had shown that these two populations differed significantly in vocalization structure. The translocated marmosets were still housed in their original social group, but after translocation they were surrounded by the vocalizations from neighbouring groups of the new population. The vocal distance between the translocated individuals and the new population decreased for two out of three call types over 16 weeks. Thus, even without direct social contact or interaction, the vocalizations of the translocated animals converged towards the new population, indicating that common marmosets can modify their calls due to acoustic input from conspecifics alone, via crowd vocal learning. To our knowledge, this is the first study able to distinguish between different explanations for vocal dialects as well as to show crowd vocal learning in a primate species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0222486PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6808547PMC
March 2020

A Simple Procedure for Creating Scalable Phenotypic Screening Assays in Human Neurons.

Sci Rep 2019 06 21;9(1):9000. Epub 2019 Jun 21.

The Scripps Research Molecular Screening Center, Department of Molecular Medicine, Scripps Research, Jupiter, Florida, 33458, USA.

Neurons created from human induced pluripotent stem cells (hiPSCs) provide the capability of identifying biological mechanisms that underlie brain disorders. IPSC-derived human neurons, or iNs, hold promise for advancing precision medicine through drug screening, though it remains unclear to what extent iNs can support early-stage drug discovery efforts in industrial-scale screening centers. Despite several reported approaches to generate iNs from iPSCs, each suffer from technological limitations that challenge their scalability and reproducibility, both requirements for successful screening assays. We addressed these challenges by initially removing the roadblocks related to scaling of iNs for high throughput screening (HTS)-ready assays. We accomplished this by simplifying the production and plating of iNs and adapting them to a freezer-ready format. We then tested the performance of freezer-ready iNs in an HTS-amenable phenotypic assay that measured neurite outgrowth. This assay successfully identified small molecule inhibitors of neurite outgrowth. Importantly, we provide evidence that this scalable iN-based assay was both robust and highly reproducible across different laboratories. These streamlined approaches are compatible with any iPSC line that can produce iNs. Thus, our findings indicate that current methods for producing iPSCs are appropriate for large-scale drug-discovery campaigns (i.e. >10e compounds) that read out simple neuronal phenotypes. However, due to the inherent limitations of currently available iN differentiation protocols, technological advances are required to achieve similar scalability for screens that require more complex phenotypes related to neuronal function.
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http://dx.doi.org/10.1038/s41598-019-45265-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6588600PMC
June 2019

The slow ape: High infant survival and long interbirth intervals in wild orangutans.

J Hum Evol 2018 12 25;125:38-49. Epub 2018 Oct 25.

Department of Anthropology, University of Zürich, Winterthurerstr 190, 8057, Zürich, Switzerland.

Orangutans (Pongo spp.) are reported to have extremely slow life histories, including the longest average interbirth intervals of all mammals. Such slow life history can be viable only when unavoidable mortality is kept low. Thus, orangutans' survivorship under natural conditions is expected to be extremely high. Previous estimates of orangutan life history were based on captive individuals living under very different circumstances or on small samples from wild populations. Here, we combine birth data from seven field sites, each with demographic data collection for at least 10 years (range 12-43 years) on wild orangutans to better document their life history. Using strict criteria for data inclusion, we calculated infant survival, interbirth intervals and female age at first reproduction, across species, subspecies and islands. We found an average closed interbirth interval of 7.6 years, as well as consistently very high pre-weaning survival for males and females. Female survival of 94% until age at first birth (at around age 15 years) was higher than reported for any other mammal species under natural conditions. Similarly, annual survival among parous females is very high, but longevity remains to be estimated. Current data suggest no major life history differences between Sumatran and Bornean orangutans. The high offspring survival is remarkable, noting that modern human populations seem to have reached the same level of survival only in the 20th century. The orangutans' slow life history illustrates what can be achieved if a hominoid bauplan is exposed to low unavoidable mortality. Their high survival is likely due to their arboreal and non-gregarious lifestyle, and has allowed them to maintain viable populations, despite living in low-productivity habitats. However, their slow life history also implies that orangutans are highly vulnerable to a catastrophic population crash in the face of drastic habitat change.
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http://dx.doi.org/10.1016/j.jhevol.2018.09.004DOI Listing
December 2018

Male monkeys use punishment and coercion to de-escalate costly intergroup fights.

Proc Biol Sci 2018 06;285(1880)

Anthropological Institute and Museum, University of Zurich, Winterthurerstrasse 190, Zurich 8057, Switzerland.

In numerous social species, males direct aggression towards female group members during intergroup fights, and this behaviour is commonly thought to function as mate guarding, even though males often target non-receptive females. In studying intergroup fights in a wild population of vervet monkeys, we found that male intragroup aggression was primarily directed towards individuals who had either just finished exhibiting, or were currently attempting to instigate intergroup aggression. Targeted females were less likely to instigate intergroup aggression in the future, indicating that male intragroup aggression functioned as coercion (when directed towards those who were currently trying to instigate a fight) and punishment (when directed towards those who had recently fought). These manipulative tactics effectively prevented intergroup encounters from escalating into fights and often de-escalated ongoing conflicts. Males who were likely sires were those most likely to use punishment/coercion, particularly when they were wounded, and, therefore, less able to protect vulnerable offspring should a risky intergroup fight erupt. This work, along with our previous finding that females use punishment and rewards to recruit males into participating in intergroup fights, highlights the inherent conflict of interest that exists between the sexes, as well as the role that social incentives can play in resolving this conflict. Furthermore, unlike other studies which have found punishment to be used asymmetrically between partners, these works represent a novel example of reciprocal punishment in a non-human animal.
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http://dx.doi.org/10.1098/rspb.2017.2323DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6015864PMC
June 2018

The social organization of Homo ergaster: Inferences from anti-predator responses in extant primates.

J Hum Evol 2017 08 7;109:11-21. Epub 2017 Jun 7.

Anthropological Institute and Museum, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland.

Patterns of primate socioecology have been used to suggest that the first truly savanna-dwelling hominin, Homo ergaster, lived in sizeable groups. Here, we revisit these estimates and infer additional features of the social organization of these early hominins based on anti-predator responses observed across the primate taxon. We first show that the effect of habitat on primate group size, composition, and sexual dimorphism is negligible after controlling for substrate use and phylogeny: terrestrial species live in larger groups with more and bigger males than arboreal taxa. We next hypothesize that groups can only survive in open habitats if males are able to engage in joint counter-attacks against the large carnivorans typical of such environments. To test this, we analyze reports on primate counter-attacks against known predators and find these are indeed disproportionately frequent in terrestrial taxa living in open habitats, sometimes even involving the use of tentative weapons. If we subsequently only examine the taxa that are particularly adept at this (chimpanzees and baboons), we find an effect of habitat type on group size: groups on the savanna are larger than those in the forest. We thus infer that H. ergaster lived in very large groups with many males that jointly defended the group against carnivorans, and argue that these counter-attacks will readily have turned into confrontational scavenging and cooperative hunting, allowing Homo to move into the niche of social carnivore. These two features (life in very large multi-male groups and a switch to persistent carnivory) shaped the evolution of our lineage to such an extent that the social organization of H. ergaster may already have contained many key elements characterizing modern day foragers: male bonding, incipient male-female friendships with food sharing, a tendency toward endogamy, and the presence of large communities that eventually turned into the ethno-linguistic units we can still recognize today.
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http://dx.doi.org/10.1016/j.jhevol.2017.05.003DOI Listing
August 2017

First integrative trend analysis for a great ape species in Borneo.

Sci Rep 2017 07 7;7(1):4839. Epub 2017 Jul 7.

The Nature Conservancy (TNC) Indonesia, Jakarta, Indonesia.

For many threatened species the rate and drivers of population decline are difficult to assess accurately: species' surveys are typically restricted to small geographic areas, are conducted over short time periods, and employ a wide range of survey protocols. We addressed methodological challenges for assessing change in the abundance of an endangered species. We applied novel methods for integrating field and interview survey data for the critically endangered Bornean orangutan (Pongo pygmaeus), allowing a deeper understanding of the species' persistence through time. Our analysis revealed that Bornean orangutan populations have declined at a rate of 25% over the last 10 years. Survival rates of the species are lowest in areas with intermediate rainfall, where complex interrelations between soil fertility, agricultural productivity, and human settlement patterns influence persistence. These areas also have highest threats from human-wildlife conflict. Survival rates are further positively associated with forest extent, but are lower in areas where surrounding forest has been recently converted to industrial agriculture. Our study highlights the urgency of determining specific management interventions needed in different locations to counter the trend of decline and its associated drivers.
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http://dx.doi.org/10.1038/s41598-017-04435-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5501861PMC
July 2017

Orientation toward humans predicts cognitive performance in orang-utans.

Sci Rep 2017 01 9;7:40052. Epub 2017 Jan 9.

Anthropological Institute and Museum, University of Zurich, Switzerland.

Non-human animals sometimes show marked intraspecific variation in their cognitive abilities that may reflect variation in external inputs and experience during the developmental period. We examined variation in exploration and cognitive performance on a problem-solving task in a large sample of captive orang-utans (Pongo abelii &P. pygmaeus, N = 103) that had experienced different rearing and housing conditions during ontogeny, including human exposure. In addition to measuring exploration and cognitive performance, we also conducted a set of assays of the subjects' psychological orientation, including reactions towards an unfamiliar human, summarized in the human orientation index (HOI), and towards novel food and objects. Using generalized linear mixed models we found that the HOI, rather than rearing background, best predicted both exploration and problem-solving success. Our results suggest a cascade of processes: human orientation was accompanied by a change in motivation towards problem-solving, expressed in reduced neophobia and increased exploration variety, which led to greater experience, and thus eventually to higher performance in the task. We propose that different experiences with humans caused individuals to vary in curiosity and understanding of the physical problem-solving task. We discuss the implications of these findings for comparative studies of cognitive ability.
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http://dx.doi.org/10.1038/srep40052DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5220318PMC
January 2017

Female monkeys use both the carrot and the stick to promote male participation in intergroup fights.

Proc Biol Sci 2016 Nov;283(1843)

Anthropological Institute and Museum, University of Zurich, Zurich, Switzerland.

Group-level cooperation often poses a social dilemma in which joint action may be difficult to achieve. Theoretical models and experimental work on humans show that social incentives, such as punishment of defectors and rewarding of cooperators, can promote cooperation in groups of unrelated individuals. Here, we demonstrate that these processes can operate in a non-human animal species, and be used to effectively promote the production of a public good. We took advantage of the fact that intergroup fights in vervet monkeys (Chlorocebus aethiops pygerythrus) are characterized by episodes of intergroup aggression with pauses in-between. During pauses, females selectively groomed males that had participated in the previous aggressive episode, but aggressed male group members that had not. In subsequent (i.e. future) episodes, males who had received either aggression or grooming participated above their personal base-line level. Therefore, female-male aggression and grooming both appear to function as social incentives that effectively promote male participation in intergroup fights. Importantly, females stood to gain much from recruiting males as the probability of winning intergroup fights was dependent on the number of active participants, relative to the number of fighters in the opposing group. Furthermore, females appear to maximize the benefits gained from recruiting males as they primarily used social incentives where and when high-quality food resources, which are the resources primarily limiting to female fitness, were at stake.
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http://dx.doi.org/10.1098/rspb.2016.1817DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5136586PMC
November 2016

Male food defence as a by-product of intersexual cooperation in a non-human primate.

Sci Rep 2016 10 24;6:35800. Epub 2016 Oct 24.

Anthropological Institute and Museum, University of Zurich, Winterthurerstrasse 190, Zurich 8057, Switzerland.

Males in a number of group-living species fight in intergroup conflicts to defend access to food resources, a seemingly paradoxical behaviour, given that this resource does not usually limit male fitness directly. We investigated the mechanism(s) driving apparent male food defence in wild vervet monkeys (Chlorocebus aethiops pygerythrus) by testing the effect that female resource access, and female audience size and activity had on the response of focal males during simulated intergroup encounters. Males do not appear to defend food to increase the reproductive success of female group members because their response was not influenced by the presence of provisioning boxes that only females could access. Female audience size was also unimportant, suggesting males do not participate in intergroup encounters to advertise their quality to potential mates. However, focal males almost always followed/supported female group members who initiated an approach towards simulated intruders, supporting that male participation largely functions to gain status as a cooperative group member, and that apparent male food defence in this species arises as a by-product of intersexual cooperation. Our study highlights that considering audience composition and activity can reveal the presence of social incentives and illuminate the evolutionary mechanism(s) promoting joint action in intergroup aggression.
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http://dx.doi.org/10.1038/srep35800DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5075891PMC
October 2016

Cognitive differences between orang-utan species: a test of the cultural intelligence hypothesis.

Sci Rep 2016 07 28;6:30516. Epub 2016 Jul 28.

Anthropological Institute &Museum, University of Zurich, Switzerland.

Cultural species can - or even prefer to - learn their skills from conspecifics. According to the cultural intelligence hypothesis, selection on underlying mechanisms not only improves this social learning ability but also the asocial (individual) learning ability. Thus, species with systematically richer opportunities to socially acquire knowledge and skills should over time evolve to become more intelligent. We experimentally compared the problem-solving ability of Sumatran orang-utans (Pongo abelii), which are sociable in the wild, with that of the closely related, but more solitary Bornean orang-utans (P. pygmaeus), under the homogeneous environmental conditions provided by zoos. Our results revealed that Sumatrans showed superior innate problem-solving skills to Borneans, and also showed greater inhibition and a more cautious and less rough exploration style. This pattern is consistent with the cultural intelligence hypothesis, which predicts that the more sociable of two sister species experienced stronger selection on cognitive mechanisms underlying learning.
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http://dx.doi.org/10.1038/srep30516DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4964338PMC
July 2016

Communal range defence in primates as a public goods dilemma.

Philos Trans R Soc Lond B Biol Sci 2015 Dec;370(1683):20150003

Anthropological Institute and Museum, University of Zurich, Winterthurerstrasse 190, Zurich 8057, Switzerland Inkawu Vervet Project, Mawana Game Reserve, KwaZulu-Natal, South Africa.

Classic socio-ecological theory holds that the occurrence of aggressive range defence is primarily driven by ecological incentives, most notably by the economic defendability of an area or the resources it contains. While this ecological cost-benefit framework has great explanatory power in solitary or pair-living species, comparative work on group-living primates has always found economic defendability to be a necessary, but not sufficient condition to account for the distribution of effective range defence across the taxon. This mismatch between theory and observation has recently been ascribed to a collective action problem among group members in, what is more informatively viewed as, a public goods dilemma: mounting effective defence of a communal range against intrusions by outgroup conspecifics. We here further develop this framework, and report on analyses at three levels of biological organization: across species, across populations within a single lineage and across groups and individuals within a single population. We find that communal range defence in primates very rarely involves collective action sensu stricto and that it is best interpreted as the outcome of opportunistic and strategic individual-level decisions. Whether the public good of a defended communal range is produced by solitary, joint or collective action is thus the outcome of the interplay between the unique characteristics of each individual, local and current socio-ecological conditions, and fundamental life-history traits of the species.
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http://dx.doi.org/10.1098/rstb.2015.0003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4633841PMC
December 2015

Endocrinological correlates of male bimaturism in wild Bornean orangutans.

Am J Primatol 2015 Nov 31;77(11):1170-8. Epub 2015 Jul 31.

Anthropological Institute and Museum, University of Zurich, Switzerland.

Among primates, orangutans are unique in having pronounced male bimaturism leading to two fully adult morphs that differ in both physical appearance and behavior. While unflanged males have a female-like appearance, flanged males have the full suite of secondary sexual characteristics, including cheek flanges and a large throat sac. So far, hormonal correlates of arrested development in unflanged males and the expression of secondary sexual characteristics in flanged males have only been studied in zoo-housed individuals. In this study, we investigated fecal androgen and glucocorticoid metabolites as hormonal correlates of male bimaturism in 17 wild adult Bornean orangutans (Pongo pygmaeus) in Central Kalimantan, Indonesia. We predicted and found higher androgen levels in flanged males compared to unflanged males, probably due to ongoing strong competition among flanged males who meet too infrequently to establish a clear linear dominance hierarchy. Furthermore, we found no difference in fecal glucocorticoid metabolite concentrations between flanged and unflanged males, indicating that social stress is unlikely to explain arrested development in unflanged wild orangutans. The only actively developing male in our study showed significantly higher androgen levels during the period of development than later as a fully flanged male. This supports earlier findings from zoo studies that elevated androgen levels are associated with the development of secondary sexual characteristics.
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http://dx.doi.org/10.1002/ajp.22453DOI Listing
November 2015

Deriving movement properties and the effect of the environment from the Brownian bridge movement model in monkeys and birds.

Mov Ecol 2015 15;3(1):18. Epub 2015 Jun 15.

Anthropological Institute & Museum, University of Zurich, Zurich, Switzerland.

Background: The Brownian bridge movement model (BBMM) provides a biologically sound approximation of the movement path of an animal based on discrete location data, and is a powerful method to quantify utilization distributions. Computing the utilization distribution based on the BBMM while calculating movement parameters directly from the location data, may result in inconsistent and misleading results. We show how the BBMM can be extended to also calculate derived movement parameters. Furthermore we demonstrate how to integrate environmental context into a BBMM-based analysis.

Results: We develop a computational framework to analyze animal movement based on the BBMM. In particular, we demonstrate how a derived movement parameter (relative speed) and its spatial distribution can be calculated in the BBMM. We show how to integrate our framework with the conceptual framework of the movement ecology paradigm in two related but acutely different ways, focusing on the influence that the environment has on animal movement. First, we demonstrate an a posteriori approach, in which the spatial distribution of average relative movement speed as obtained from a "contextually naïve" model is related to the local vegetation structure within the monthly ranging area of a group of wild vervet monkeys. Without a model like the BBMM it would not be possible to estimate such a spatial distribution of a parameter in a sound way. Second, we introduce an a priori approach in which atmospheric information is used to calculate a crucial parameter of the BBMM to investigate flight properties of migrating bee-eaters. This analysis shows significant differences in the characteristics of flight modes, which would have not been detected without using the BBMM.

Conclusions: Our algorithm is the first of its kind to allow BBMM-based computation of movement parameters beyond the utilization distribution, and we present two case studies that demonstrate two fundamentally different ways in which our algorithm can be applied to estimate the spatial distribution of average relative movement speed, while interpreting it in a biologically meaningful manner, across a wide range of environmental scenarios and ecological contexts. Therefore movement parameters derived from the BBMM can provide a powerful method for movement ecology research.
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http://dx.doi.org/10.1186/s40462-015-0043-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4466871PMC
June 2015

Cholesterol-derived glucocorticoids control early fate specification in embryonic stem cells.

Stem Cell Res 2015 Jul 14;15(1):88-95. Epub 2015 May 14.

Muscle Development and Regeneration Program, Sanford-Burnham Medical Research Institute, La Jolla, CA, USA. Electronic address:

Aside from its role in cell membrane integrity, cholesterol is a key component in steroid hormone production. The vital functions of steroid hormones such as estrogen, testosterone, glucocorticoids (Gcrts) and mineralocorticoids (Mnrts) in perinatal and adult life are well understood; however, their role during early embryonic development remains largely unexplored. Here we show that siRNA-mediated perturbation of steroid hormone production during mesoderm formation has important consequences on cardiac differentiation in mouse embryonic stem cells (mESC). Both Gcrts and Mnrts are capable of driving cardiac differentiation in mESC. Interestingly, the Gcrt receptor is widely expressed during gastrulation in the mouse, and is exclusively localized in the nuclei-and thus active-in visceral endoderm cells, suggesting that it functions much earlier than previously anticipated. We therefore studied Gcrt signaling in mESC as a model of the gastrulating embryo, and found that Gcrt signaling regulates expression of the transcription factor Hnf4a and the secreted Nodal and BMP inhibitor Cer1 in the early visceral endoderm. RNAi-mediated knockdown of Gcrt function blocked cardiomyocyte differentiation, with limited effects on other cardiovascular cell types including vascular endothelial cells and smooth muscle. Furthermore, the cardiogenic effect of Gcrts required Hnf4a and paracrine Cer1. These results establish a novel function for cholesterol-derived steroid hormones and identify Gcrt signaling in visceral endoderm cells as a regulator of Cer1 and cardiac fate.
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http://dx.doi.org/10.1016/j.scr.2015.04.010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4516691PMC
July 2015

Validation of an acoustic location system to monitor Bornean orangutan (Pongo pygmaeus wurmbii) long calls.

Am J Primatol 2015 Jul 16;77(7):767-76. Epub 2015 Mar 16.

Anthropological Institute and Museum, University of Zurich, Zurich, Switzerland.

The long call is an important vocal communication signal in the widely dispersed, semi-solitary orangutan. Long calls affect individuals' ranging behavior and mediate social relationships and regulate encounters between dispersed individuals in a dense rainforest. The aim of this study was to test the utility of an Acoustic Location System (ALS) for recording and triangulating the loud calls of free-living primates. We developed and validated a data extraction protocol for an ALS used to record wild orangutan males' long calls at the Tuanan field site (Central Kalimantan). We installed an ALS in a grid of 300 ha, containing 20 SM2+ recorders placed in a regular lattice at 500 m intervals, to monitor the distribution of calling males in the area. The validated system had the following main features: (i) a user-trained software algorithm (Song Scope) that reliably recognized orangutan long calls from sound files at distances up to 700 m from the nearest recorder, resulting in a total area of approximately 900 ha that could be monitored continuously; (ii) acoustic location of calling males up to 200 m outside the microphone grid, which meant that within an area of approximately 450 ha, call locations could be calculated through triangulation. The mean accuracy was 58 m, an error that is modest relative to orangutan mobility and average inter-individual distances. We conclude that an ALS is a highly effective method for detecting long-distance calls of wild primates and triangulating their position. In combination with conventional individual focal follow data, an ALS can greatly improve our knowledge of orangutans' social organization, and is readily adaptable for studying other highly vocal animals.
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http://dx.doi.org/10.1002/ajp.22398DOI Listing
July 2015

High content screening for modulators of cardiac differentiation in human pluripotent stem cells.

Methods Mol Biol 2015 ;1263:43-61

Muscle Development and Regeneration Program, Sanford-Burnham Medical Research Institute, 10901 North Torrey Pines Road, La Jolla, CA, 92037, USA.

Chemical genomics has the unique potential to expose novel mechanisms of complex cellular biology through screening of small molecules in in vitro assays of a biological phenotype of interest, followed by target identification. In the case of disease-specific assays, the cellular proteins identified might constitute novel drug targets, and the small molecules themselves might be developed as drug leads. In cardiovascular biology, a chemical genomics approach to study the formation of cardiomyocyte, vascular endothelial, and smooth muscle lineages might contribute to therapeutic regeneration. Here, we describe methods used to develop high content screening assays implementing multipotent cardiovascular progenitors derived from human pluripotent stem cells and have identified novel compounds that direct cardiac differentiation.
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http://dx.doi.org/10.1007/978-1-4939-2269-7_4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4766105PMC
September 2015

Cyclic stretch of embryonic cardiomyocytes increases proliferation, growth, and expression while repressing Tgf-β signaling.

J Mol Cell Cardiol 2015 Feb 13;79:133-44. Epub 2014 Nov 13.

Department of Pediatrics (Cardiology), University of California San Diego, United States; Rady Children's Hospital San Diego, United States; Institute for Engineering in Medicine, University of California San Diego, United States. Electronic address:

Perturbed biomechanical stimuli are thought to be critical for the pathogenesis of a number of congenital heart defects, including Hypoplastic Left Heart Syndrome (HLHS). While embryonic cardiomyocytes experience biomechanical stretch every heart beat, their molecular responses to biomechanical stimuli during heart development are poorly understood. We hypothesized that biomechanical stimuli activate specific signaling pathways that impact proliferation, gene expression and myocyte contraction. The objective of this study was to expose embryonic mouse cardiomyocytes (EMCM) to cyclic stretch and examine key molecular and phenotypic responses. Analysis of RNA-Sequencing data demonstrated that gene ontology groups associated with myofibril and cardiac development were significantly modulated. Stretch increased EMCM proliferation, size, cardiac gene expression, and myofibril protein levels. Stretch also repressed several components belonging to the Transforming Growth Factor-β (Tgf-β) signaling pathway. EMCMs undergoing cyclic stretch had decreased Tgf-β expression, protein levels, and signaling. Furthermore, treatment of EMCMs with a Tgf-β inhibitor resulted in increased EMCM size. Functionally, Tgf-β signaling repressed EMCM proliferation and contractile function, as assayed via dynamic monolayer force microscopy (DMFM). Taken together, these data support the hypothesis that biomechanical stimuli play a vital role in normal cardiac development and for cardiac pathology, including HLHS.
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http://dx.doi.org/10.1016/j.yjmcc.2014.11.003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4302020PMC
February 2015

Whole-mount in situ hybridization (WISH) optimized for gene expression analysis in mouse embryos and embryoid bodies.

Methods Mol Biol 2014 ;1211:27-40

Department of Biology, Lab of Cell Genetics, Vrije Universiteit Brussel, Pleinlaan, 2, 1050, Brussels, Belgium,

Whole-mount in situ hybridization (WISH) is a technique widely used in developmental biology to study the localization of RNA sequences in intact tissues or whole organisms. In this chapter we present a detailed protocol that was optimized for gene expression analysis in early stage mouse embryos (5.5-10.5 days post-coitum) and embryoid bodies formed by differentiating embryonic stem cells and can be used for the detection of up to two distinct RNA sequences simultaneously. The initial steps of the procedure are the generation of the labeled riboprobe(s) and the embryo or embryoid body preparation, which can be completed in less than 2 days. The actual WISH procedure, comprised of the hybridization, the post-hybridization washes, and the immunological staining, can be completed in 3 days.
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http://dx.doi.org/10.1007/978-1-4939-1459-3_3DOI Listing
May 2015

Integrating omics into the cardiac differentiation of human pluripotent stem cells.

Wiley Interdiscip Rev Syst Biol Med 2014 Jul-Aug;6(4):311-28. Epub 2014 Apr 21.

Muscle Development and Regeneration Program, Sanford-Burnham Medical Research Institute, La Jolla, CA, USA; Department of Bioengineering, UC San Diego, La Jolla, CA, USA.

Time-dependent extracellular manipulations of human pluripotent stem cells can yield as much as 90% pure populations of cardiomyocytes. While the extracellular control of differentiation generally entails dynamic regulation of well-known pathways such as Wnt, BMP, and Nodal signaling, the underlying genetic networks are far more complex and are poorly understood. Notably, the identification of these networks holds promise for understanding heart disease and regeneration. The availability of genome-wide experimentation, such as RNA and DNA sequencing, as well as high throughput surveying with small molecule and small interfering RNA libraries, now enables us to map the genetic interactions underlying cardiac differentiation on a global scale. Initial studies demonstrate the complexity of the genetic regulation of cardiac differentiation, exposing unanticipated novel mechanisms. However, the large datasets generated tend to be overwhelming and systematic approaches are needed to process the vast amount of data to improve our mechanistic understanding of the complex biology. Systems biology methods spur high hopes for parsing vast amounts of data into genetic interaction models that can be verified experimentally and ultimately yield functional networks that expose the genetic connections underlying biological processes.
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http://dx.doi.org/10.1002/wsbm.1268DOI Listing
February 2015

Reprogramming the cardiac field.

Circ Res 2014 Jan;114(3):409-11

From The Muscle Development and Regeneration Program, Sanford-Burnham Medical Research Institute, La Jolla, CA (E.W., M.M.); and Department of Bioengineering, University of California, San Diego, San Diego, CA (M.M.).

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http://dx.doi.org/10.1161/CIRCRESAHA.113.302946DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4046860PMC
January 2014

Small molecules targeting in vivo tissue regeneration.

ACS Chem Biol 2014 Jan 6;9(1):57-71. Epub 2014 Jan 6.

Faculty of Chemistry & Chemical Biology, TU Dortmund University , Otto-Hahn-Str. 6, 44227 Dortmund, Germany.

The field of regenerative medicine has boomed in recent years thanks to milestone discoveries in stem cell biology and tissue engineering, which has been driving paradigm shifts in the pharmacotherapy of degenerative and ischemic diseases. Small molecule-mediated replenishment of lost and/or dysfunctional tissue in vivo, however, is still in its infancy due to a limited understanding of mechanisms that control such endogenous processes of tissue homeostasis or regeneration. Here, we discuss current progress using small molecules targeting in vivo aspects of regeneration, including adult stem cells, stem cell niches, and mechanisms of homing, mobilization, and engraftment as well as somatic cell proliferation. Many of these compounds derived from both knowledge-based design and screening campaigns, illustrating the feasibility of translating in vitro discovery to in vivo regeneration. These early examples of drug-mediated in vivo regeneration provide a glimpse of the future directions of in vivo regenerative medicine approaches.
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http://dx.doi.org/10.1021/cb4008277DOI Listing
January 2014

Coordinate Nodal and BMP inhibition directs Baf60c-dependent cardiomyocyte commitment.

Genes Dev 2013 Nov;27(21):2332-44

Sanford-Burnham Medical Research Institute, La Jolla, California 92037, USA;

A critical but molecularly uncharacterized step in heart formation and regeneration is the process that commits progenitor cells to differentiate into cardiomyocytes. Here, we show that the endoderm-derived dual Nodal/bone morphogenetic protein (BMP) antagonist Cerberus-1 (Cer1) in embryonic stem cell cultures orchestrates two signaling pathways that direct the SWI/SNF chromatin remodeling complex to cardiomyogenic loci in multipotent (KDR/Flk1+) progenitors, activating lineage-specific transcription. Transient inhibition of Nodal by Cer1 induces Brahma-associated factor 60c (Baf60c), one of three Baf60 variants (a, b, and c) that are mutually exclusively assembled into SWI/SNF. Blocking Nodal and BMP also induces lineage-specific transcription factors Gata4 and Tbx5, which interact with Baf60c. siRNA to Cer1, Baf60c, or the catalytic SWI/SNF subunit Brg1 prevented the developmental opening of chromatin surrounding the Nkx2.5 early cardiac enhancer and cardiomyocyte differentiation. Overexpression of Baf60c fully rescued these deficits, positioning Baf60c and SWI/SNF function downstream from Cer1. Thus, antagonism of Nodal and BMP coordinates induction of the myogenic Baf60c variant and interacting transcription factors to program the developmental opening of cardiomyocyte-specific loci in chromatin. This is the first demonstration that cues from the progenitor cell environment direct the subunit variant composition of SWI/SNF to remodel the transcriptional landscape for lineage-specific differentiation.
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http://dx.doi.org/10.1101/gad.225144.113DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3828519PMC
November 2013

The need for transparency and good practices in the qPCR literature.

Nat Methods 2013 Nov;10(11):1063-7

Postgraduate Medical Institute, Anglia Ruskin University, Chelmsford, UK.

Two surveys of over 1,700 publications whose authors use quantitative real-time PCR (qPCR) reveal a lack of transparent and comprehensive reporting of essential technical information. Reporting standards are significantly improved in publications that cite the Minimum Information for Publication of Quantitative Real-Time PCR Experiments (MIQE) guidelines, although such publications are still vastly outnumbered by those that do not.
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http://dx.doi.org/10.1038/nmeth.2697DOI Listing
November 2013

Jumonji and cardiac fate.

Circ Res 2013 Sep;113(7):837-9

From the Muscle Development and Regeneration Program, Sanford-Burnham Medical Research Institute, La Jolla, CA.

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http://dx.doi.org/10.1161/CIRCRESAHA.113.302202DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3974910PMC
September 2013