Previous Research
Before the application of genetic tools for the assessment of paternity, kinship in primates was only studied with respect to maternal kinship. Since the first studies incorporated the knowledge about paternal kinship, our knowledge about the impact of paternal kinship upon the evolution of social behavior has greatly improved (e.g., wild savanna baboons: Alberts 1999, Smith et al. 2003, Buchan et al. 2003, Silk et al. 2006, van Horn et al. 2007, Charpentier et al. 2008; free-ranging rhesus macaques: Widdig et al. 2001, 2002, 2004, 2006a, b; free-ranging mandrills: Charpentier et al. 2007). Today we have strong evidence that female Cercopithecines are capable to recognize their paternal kin as they preferentially interact with paternal half-sisters when compared to unrelated females in different social context (see Widdig 2007 for review).
Current Research
Paternity projects
The first set of question of the Junior Research Group is to expand our knowledge of paternity in some specific projects outline below.
1. Development of paternal kin bias
In this long-term study we are going to test the mechanisms underlying paternal kin discrimination. The most likely mechanisms are familiarity and phenotype matching. Most studies on paternal kin recognition suggested phenotype matching, but did not test for all sources of familiarity. We therefore following individuals from birth till they reach adulthood to understand the development of paternal kin bias. We are testing whether the mothers and/or the father mediate familiarity among paternal half-siblings.
Species/Field site: Rhesus macaques/ Cayo Santiago, Puerto Rico
Research assistants: Bianca Guira
2. Determinants of paternity skew
According to sexual selection theory, reproduction among males should vary within a population. In primates, male reproduction is often skewed towards a few successful sires within a given birth season leading to a high proportion of age-mates being paternal half-siblings. Both male and female reproductive strategies can actually lead to a skew in male reproduction either via male-male competition over access to fertile females and/or via female mate choice towards the ‘best’ mate. The relative impact of both male and female reproductive strategies during mating when conception is most likely will determine the degree of male skew and hence the availability of paternal kin within a group. This project aims to investigate to what extent female mate choice and/or male monopolization determine male reproductive skew in rhesus macaques.
Species/Field site: Rhesus macaques/ Cayo Santiago, Puerto Rico
PhD student: Constance Dubuc
Collaboration: Antje Engelhardt, Michael Heistermann
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3. What do females know about their offspring’s’ paternity?
It is common theory that females in multi-male groups mate promiscuously to confuse paternity in order to protect their offspring against infanticide. The graded signal hypothesis states that females confuse males about the day they are most likely to conceive. Lower-ranking males who have not managed to mate with a female at the time of most likely conception would still avoid attacking infants as they still have some chance of being the sire. However, to date it is unclear whether females have reliable information about their offsprings’ paternity and if they do so, whether or not they express their knowledge. To avoid infanticide mothers should hide their paternity knowledge, if indeed available, when the risk of infanticide is highest (first 12 months of offspring’s life). This is because ensuring paternity to the genetic father (via mother-father post-birth bonds) would at the same time ensure non-paternity to all other males. As a result an increasing risk of infanticide by non-fathers would likely be of higher cost to the offspring (and mother) than the potential benefit derived from the protection by the genetic father during an infanticidal attack. In this project we are investigating whether mothers express paternity knowledge of their offspring after its birth.
Species/Field site: Rhesus macaques/ Cayo Santiago, Puerto Rico
Collaboration: Lauren Brent
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4. Do social bonds of paternal half-siblings vary according to the strength of male reproductive skew?
Previous studies have shown that male reproduction is highly skewed in many primate species. The most important consequence of this skew in terms of kin relationships within groups is that age mates tend to be paternal half-siblings. Adult females have been shown to form stronger social bonds with their paternal half-sisters than with unrelated females. However, male skew can vary across groups and years depending upon factors such as group size, number of potential sires, stability of the male hierarchy. Here, we study the variation in skew and how this affects the strength of social bonds in rhesus macaques.
Species/Field site: Rhesus macaques/ Cayo Santiago, Puerto Rico
Collaboration: Lauren Brent
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5. Paternal care in Sulawesi black crested macaques
Female primates mate with multiple partners during likely conception to confuse paternity in order to minimize the risk of infanticide. Previous studies have demonstrated that male group members present at the time of the infants’ conception are less likely to attack infants than males immigrating after the infants’ conception. As males always face some uncertainty of paternity even when they mate-guarded a given female for most of her cycle, it is still not clear whether or not male primates are able to recognize their own offspring and if so, whether males provide paternal care. In Sulawesi black crested macaques mortality and/or injuries of newborns are frequent and injured newborns are protected by certain males. The aim of our project is to study male-offspring interaction in this species to understand whether males indeed provide paternal care to offspring during infanticide attacks and what mechanism males use to identify their offspring.
Species/Field site: Sulawesi black crested macaques/ Tangkoko-Bataungus Nature Reserve, Indonesia
PhD student: Daphné Kerhoas
Collaboration: Antje Engelhardt
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6. Male fitness: Achievement and maintenance of dominance in male Sulawesi black crested macaques
Male of high dominance status are known to sire more offspring than males of low dominance status. However, it is less studied how male achieve and maintain high rank. The aim of this study is to examine the determinants of a male’s position within a group’s dominance hierarchy in wild Sulawesi black crested macaques. This study will address the following questions: (1) Do individual features, such as age, kin availability, body condition, characteristics of sexual signals and/or personality affect a male’s dominance rank. (2) How important are male coalition partners for the achievement and maintenance of high dominance status. (3) How important is female support for the achievement and maintenance of high dominance status. Finally, how stable are male hierarchies in time.
Species/Field site: Sulawesi black crested macaques/ Tangkoko-Bataungus Nature Reserve, Indonesia
PhD student: Christof Neumann
Collaboration: Antje Engelhardt
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7. Do males recognize their paternal half-siblings?
Evidence for paternal kin bias is limited to females who remain in their natal group in most primate species. Given the high (but not perfect) skew in male reproduction females therefore interact continuously with both kin and non-kin throughout their lives. In contrast, many male primates leave their natal group around puberty to join a different social group for breeding. Therefore, males are thought to be less likely to interact with kin once they migrate, but this prediction has never been tested for paternal kin. As males successfully reproduce across different groups, we found paternal half-siblings to be born either in the same or different social groups. Since dispersal is associated with high costs (e.g., mortality, starvation), it is predicted that males could reduce dispersal costs by migrating together with a paternal half-brother either familiar (born in same group) or unfamiliar (born in different groups). Likewise, it is predicted that dispersing males should avoid dispersing into groups containing many close female paternal kin. This project aims at testing these predictions on a large data set of the Cayo Santiago macaque population.
Species/Field site: Rhesus macaques/ Cayo Santiago, Puerto Rico
Post-doc: Laura Muniz
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Which cues use primates to identify their paternal kin?
The second aim of this Junior Research Group is to study potential cues which might be used by primates to identify their paternal kin.
1. Odor as a cue
If primates use odor to identify paternal kin, we would expect to find individual odor pattern persistent over time. Furthermore, individual odor pattern are expected to show higher similarity (or smaller variations) between paternal kin than between non-kin. To show that primates use odor to identify paternal kin, we will investigate whether monkeys give a differential behavioral response when being exposed to kin or non-kin odor (Bioassay test).
Species/Field site: Rhesus macaques/ Cayo Santiago, Puerto Rico
Collaboration: Christine Drea
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2. Appearance
When animals use appearance as a cue to assess paternal kinship in others, we predict that paternal kin share more visual cues than unrelated individuals. To test this hypothesis we collected high quality standardized images of individuals of known kinship. As a control, we collected images of non-kin for whom we matched of age and sex. Use of human assessors offers the quickest and most cost-effective method of gaining insight into whether reliable facial cues exist. Human subjects will be tested using an automated procedure, in which stimuli are displayed on a color computer monitor and responses indicated via the keyboard. Alternatively, we are looking for face recognition software which would allow us to quantify facial similarities.
Species/Field site: Rhesus macaques/ Cayo Santiago, Puerto Rico
Collaboration: Ani Kazem
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3. Acoustics
If animals use acoustic characteristics as a cue to assess paternal kinship, we would first need to demonstrate that paternal kin share more acoustic characteristics than unrelated individuals. If such patterns can be observed, we aim to test whether individuals indeed use vocal cues to recognize paternal kin. For example, we would predict that test subjects respond different to playback calls of paternal half-siblings than to playback calls of non-kin.
Species/Field site: Rhesus macaques/ Cayo Santiago, Puerto Rico
Postdoc: Dana Pfefferle
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4. Personality
To examine whether personality is a cue used in paternal kin discrimination we asked current research assistants who are well acquainted with individual monkeys to assess the personality of the monkeys using newly developed personality inventories. We will compare correlations among the personality factors of pairs of paternal kin to unrelated pairs. While this is not a direct measure of heritability, it should show whether individuals who share a father are more like one another than those who do not.
Species/Field site: Rhesus macaques/ Cayo Santiago, Puerto Rico
Collaboration: Jana Uher
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References:
Alberts, SC (1999). Paternal kin discrimination in wild baboons. Proceedings of the Royal Society London B 266, 1501-1506.
Buchan JC, Alberts SC, Silk JB, Altmann J (2003). True paternal care in a multi-male primate society. Nature 425, 179-181.
Charpentier MJE, Peignot P, Hossaert-Mckey M, Wickings JE (2007). Kin discrimination in juvenile Mandrills (Mandrillus sphinx). Animal Behaviour 73, 37-45.
Charpentier MJ E, Van Horn RC, Altmann J, Alberts SC (2008). Paternal effects on offspring fitness in a multimale primate society. Proceedings of the National Academy of Science U.S.A. 105, 1988-1992.
Silk JB, Altmann J, Alberts SC (2006). Social relationships among adult female baboons (Papio cynocephalus). I. Variation in the strength of social bonds. Behavioral Ecology and Sociobiology 61, 183-195.
Smith KL, Alberts SC, Altmann J (2003). Wild female baboons bias their social behaviour towards paternal half-sisters. Proceedings of the Royal Society of London, Series B, 270, 503-510.
Van Horn, RC, Buchan JC, Altmann J, Alberts SC (2007). Divided destinies: group choice by female savannah baboons during social group fission. Behavioral Ecology and Sociobiology 61, 1823-1837.
Widdig A (2002). Paternal kinship among adult female rhesus macaques (Macaca mulatta). PhD thesis, Humboldt University Berlin.http://edoc.hu-berlin.de/dissertationen/widdig-anja-2002-07-17/.
Widdig A (2007). Paternal kin discrimination: the evidence and likely mechanisms. Biological Reviews 82, 319-334.
Widdig A, Bercovitch FB, Streich WJ, Nürnberg P, Krawczak M ( 2004). A longitudinal analysis of reproductive skew in male rhesus macaques. Proceedings of the Royal Society London B 271, 819-826.
Widdig A, Nürnberg P, Bercovitch FB, Trefilov A, Berard JB, Kessler MJ, Schmidtke J, Streich JW, Krawczak M (2006a). Consequences of group fission for the patterns of relatedness among rhesus macaques. Molecular Ecology 15, 3825-2832.
Widdig A, Nürnberg P, Krawczak M, Streich WJ, Bercovitch FB (2001). Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. Proceedings of the National Academy of Science U.S.A. 98, 13769-13773.
Widdig A, Nürnberg P, Krawczak M, Streich WJ, Bercovitch FB (2002). Affiliation and aggression among adult female rhesus macaques: a genetic analysis of paternal cohorts. Behaviour 139, 371-391.
Widdig A, Streich WJ, Nürnberg P, Croucher PJP, Bercovitch FB, Krawczak M (2006b). Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta). Behavioral Ecology and Sociobiology 61, 205-214.
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