Frances J. White - Research Interests

(curriculum vitae)

As a primate behavioral ecologist, my research focuses on the ecological and social factors important in the evolution of primate social systems. I am interested in the evolutionary costs and benefits of female sociality and the interplay of male and female social strategies. I have addressed these theoretical questions through field studies on wild pygmy chimpanzees (Pan paniscus) and wild and captive populations of several species of prosimian primates, primarily ruffed lemurs (Varecia variegata), ring-tailed lemurs (Lemur catta), and brown lemurs (Eulemur fulvus). I have also used molecular methods of DNA fingerprinting for paternity and maternity exclusion to examine the evolutionary consequences of different male and female social strategies. Below I have summarized my major research projects in which I am the sole or first Principal Investigator.

1) The Lomako Forest Pygmy Chimpanzee Project: female behavior, ecology, and genetics (sole P.I.)

Female sociality in pygmy chimpanzees (Pan paniscus) is unique among primates. Not only is this the only ape with female-bonding, but this bonding appears to be among non-relatives. Pan paniscus also shows female feeding priority without female social dominance: a trait found in only one other species to date. My research on the pygmy chimpanzees in the Lomako Forest of central Democratic Republic of the Congo is funded by the National Science Foundation, the L. S. B. Leakey Foundation, and other sources. I am examining the uniqueness of female sociality of pygmy chimpanzees on three main fronts centered on questions of behavior, ecology, and genetics. My current research on behavior focuses on the evolution of female feeding priority and male deference, research on ecology focuses on the key ecological correlates important in the evolution of the female-based social system, and research on genetics focuses primarily on the degree of relatedness among bonded females in two adjacent communities.

a) Female feeding priority, male deference, and female choice

It is rare for a female mammal to dominate a conspecific male.  Males are often bigger or better fighters than females, presumably because traits associated with male competitive success such as larger body size and fighting ability are favored by sexual selection. My data from 1983 through 1998 demonstrate that pygmy chimpanzees show female feeding priority without female social dominance. Males are clearly social dominant, as all adult and sub-adult males outrank all females. I have found, however, that pygmy chimpanzees females, feed more than males. These differences in feeding success are due in part to male-male competition, as suggested by cases in which males did not enter the food tree or left early following aggressive exclusion by a dominant male. These exclusions are associated with competition for mating opportunities. However, not all sex differences in feeding can be attributed to male-male competition for mating opportunities. Some differences reflect male deference to females in a feeding context.

Male deference despite male aggressive superiority implies a strong element of female choice. In large food patches, feeding competition is reduced and females can form social groups where female coalitions become possible. Where females can form coalitions to out-rank males, there is less opportunity for sexual coercion and more opportunity for female choice to operate. Female feeding priority in pygmy chimpanzees may, therefore, reflect male strategies to increase reproductive success through increased access to females. Males could influence female mate choice by allowing them to feed first. Females would then choose males based on this deference. This may be similar to the sex-for-food phenomenon which has been observed in provisioned and captive groups, where sharing or transfer of provisioned food from males to females was associated with mating.

b) Ecological basis of the female-based social system

The two species of chimpanzee, P. troglodytes and Pan paniscus, have drastically different social systems. Pan troglodytes is male-bonded, whereas my research on the pygmy chimpanzee shows a female-biased social system with little affiliation among the males and strong affiliation among females. The close social bonding among females includes the unique female homosexual behavior of genito-genital (GG) rubbing. GG-rubbing highlights the ecological basis of female affiliation in this species through the strong relationship of this behavior with feeding, levels of feeding competition, and potential cooperative defense of food. Earlier examinations of the differences in social organization of chimpanzees and pygmy chimpanzees supported my hypothesis that pygmy chimpanzees have a reduced level of feeding competition that permits larger parties. However, more recently in a test of these ecological parameters for rain forest chimpanzees at Kibale, collaborators Dr. Colin Chapman, University of Florida, and Richard Wrangham, Harvard University, and I found that Kibale Forest chimpanzees used patch sizes that were comparable to those at Lomako even though female-female affiliation at Kibale was similar to other populations of P. troglodytes. We concluded that variation in the levels of competition throughout the year may be the most important factor in determining inter-species differences in social bonding.

This interpretation that social differences are correlated with differences in variation experienced by the species is supported by my recent comparisons of the variation in monthly mean party size. My results show that there is more variation in Pan troglodytes food abundance and distribution than experienced by Pan paniscus, suggesting that it is the level of variation in food availability rather than the absolute amount, that is the critical difference selecting for the difference in social organization between the two species.

My research now focuses on the hypothesis that the crucial difference between female-based P. paniscus and male-bonded P. troglodytes is that pygmy chimpanzees do not undergo a crunch period which makes large parties are unfeasible. My next project in this topic will examine periods of low food availability to determine the impact of food shortage on the ability of individuals to remain together. This will require detailed phenological monitoring of food availability and distribution to determine the impact of food shortage on sociality in pygmy chimpanzees.

c) Genetic relatedness within communities

A trait that is common among apes, and has also been identified as a possible ancestral human condition, is that of female transfer. Female transfer has now been observed in the wild at both Lomako and at the provisioned site of Wamba. Because females transfer between communities, adult females within a community will be unrelated. Males, in contrast, remain in their natal community and often retain a strong tie with their mothers. The dominance rankings of adult males are strongly influenced by the presence of their mothers in the community. Therefore, pygmy chimpanzees may prove to represent the unique situation of female-bonding without female relatedness combined with male relatedness without male-bonding.

My research examining the relatedness among wild pygmy chimpanzees using non-invasive DNA sampling and multilocus genotyping using hypervariable nuclear loci received initial funding from NSF. The first samples of DNA were collected in the field from buccal cells in wadges (chewed plant material). These small amounts of DNA are amplified in the laboratory by PCR and probed. The long term goals of this research was to determine whether this species shows: 1) the unique situation of female-bonding among non-relatives, 2) social groups containing male relatives without male-bonding, and 3) significant influence of mothers on adult male social rank. However the political instability in the Democratic Republic of the Congo meant that this research has had to be postponed to some future date.

2) Female-female relationships, male parental care and the threat of infanticide in Varecia (sole P.I.)

My research on ruffed lemurs (Varecia variegata variegata and V. v. rubra) includes field studies in Madagascar, studies of free-ranging animals on St. Catherine’s Island, GA, and captive studies at the Duke University Primate Center. It currently is funded by the American Museum of Natural History and other sources.

Ruffed lemurs present a unique set of female behavioral and ecological traits. As specialized frugivores, individuals typically have large, defended home ranges. The female reproductive strategy involves keeping infants in nests that the female guards for the first few weeks of life, thus restricting her ranging during this time. This strategy of shareable care (guarding) as opposed to non-shareable care (carrying offspring) has allowed Varecia to produce up to four infants per litter instead of the more typical single births of primates of this size.

The social organization of this species is especially interesting as it is first characterized by highly flexible sociality: groups vary from stable pair-bonds to what have been described as fission-fusion communities and inter-individual cohesion is highly variable. My studies have suggested an explanation for the variation in social organization of groups. I have found that female-female relationships are unusual in this species, in that maturing daughters consistently outrank their mothers and may even evict them from social groups if no other options are available. However, my recent results suggest that this behavior actually reflects a strategy of female inheritance of territories that is tied to the invasion by the mother of an established territory elsewhere. Established territories are preferred due to the need for a breeding male to guard offspring, primarily against infanticide. This strategy of invasion and inheritance explains the significantly biased sex-ratio at birth observed for females of different ages. Over time this strategy would expand a pair-bonded group to produce the fission-fusion network of related females with neighboring territories that has been found for some populations.

Infanticide and the threat of infanticide are potentially powerful influences on primate social systems that have been suggested as important factors selecting for the high level of male-female associations in prosimian social groups. Infanticide by males has been observed in free-ranging ring-tailed lemurs, sifakas, and ruffed lemurs. My work with Varecia also investigates the impact of infanticide threat on male and female parental strategies, especially guarding.

Guarding is an important feature of ruffed lemur parental care. Females prepare nests before parturition away from the rest of the group. These nests are used exclusively for the care of the litter of one to four infants. At no time do infants cling to the fur or ride on any other group members. Infants can be guarded by mothers, adult males, and siblings. Guarding by male ruffed lemurs is highly variable both among individuals and by the same individual in different years. It can increase offspring survival through protection from predators and infanticide, increase access to reproductive females, or help in social interactions such as agonistic buffering. My research has examined two of these functions: guarding from predation, and guarding from infanticide.

By examining guarding behavior in social groups with different mating systems, I was able to examine the impact of infanticide threat on the variation in guarding behaviors. I found that female guarding functions primarily for predation protection and only secondarily for infanticide protection. Male guarding, in contrast, function only for infanticide protection.

My future research on this question will be to examine the influence of male parental care on female choice of mates, the role of non-breeding siblings in infant care, and establishment or inheritance of territories in this highly female-dominant species. Female choice of mates will be determined through behavioral observation and paternity will be determined using DNA fingerprinting of offspring. In my future research, I also wish to use experimental manipulations of feeding competition to examine the ecological correlates of the flexible cohesion in this species.

3) Ecological correlates of female dominance in lemurs: male deference and male agonistic rank as reproductive strategies (collaborative project)

My research on ring-tailed lemurs (in collaboration with Dr. Deborah Overdorff, University of Texas at Austin and Dr. Timothy Keith-Lucas, The University of the South) examines the evolution of female dominance and the role of male behavioral strategies in reproductive success (publications 37, 28). It has been hypothesized that female dominance in some lemur species, such as the ring-tailed lemur (Lemur catta), can be related to the high energy demands and relatively inefficient reproductive physiology of these primates in the highly seasonal environment of Madagascar. When food is limited and feeding competition is intense, females would not be able to gain sufficient food to successfully reproduce without feeding priority over males. As females are dominant in many species of lemurs, they gain first access to food resources. This female feeding priority is thought to be crucial to the adaptive significance of this social system.

Female feeding priority is, therefore, expected to be advantageous where feeding competition is strong. It is expected that as feeding competition increases, the greater will be the advantage of female feeding priority and the stronger will be the dominance hierarchy. If female dominance has evolved as hypothesized, variation in levels of feeding competition should produce variation in levels of female dominance and feeding priority.

Our feeding experiments with groups free-ranging ring-tailed lemurs (funded by the American Museum of Natural History) show strong relationships between the degree of female dominance and the level of feeding competition. However, we also found that there is a major cost to male rank in that food access decreases with increased male rank. This cost for high ranking males is, however, not a consequence of female aggression. Instead, high ranking males appear to defer to those females that have reached maturity. By doing so, these males avoid the aggressive interactions that are instead directed primarily at lower ranking males. Females are not, however, choosing “wimpy” males, as has been suggested in some cases, as these males score highest in agonistic interactions among the males. Although these high-ranking males receive less food, the major advantage appears to be that they are preferred mates. My DNA fingerprinting of one study group has confirmed that the highest ranking males sired the majority of the offspring. These results, however, were from the study of one group (on St. Catherine’s Island) that contained only 5 males, several of which were related to the breeding female, which complicated the picture of mate choice.

Our research also examines the importance of male deference in two larger, neighboring groups of ring-tailed lemurs at the Duke University Primate Center. These groups contain multiple males and females, and males often transfer between groups. This design allows to examine our hypothesis that male deference is a strategy of high ranking males to gain reproductive success. We are examining how male behavior changes as they transfer between groups and change dominance rank. The relative reproductive success of males is examined using DNA fingerprinting of infants born together with observations of active female choice during the mating season.

4) Brown lemurs and the evolution of aggressive dominance versus non-aggressive based “power” in prosimian primates (collaborative project)

This is research conducted in collaboration with Dr. Deborah Overdorff, University of Texas at Austin and Dr. Leslie Digby, Duke University.

Models of human gender differences in aggression have drawn heavily on non-human primate studies of classically male-dominant primates. It may be expected that the types and degree of aggressive interactions are dependent on the relative dominance between the sexes such that male-dominant species show higher levels of male aggression. Unlike other primates, many Madagascar lemurs are female dominant rather than male-dominant and, therefore, provide an important model for examining the importance of gender-based dominance in primates. Brown lemurs (Eulemur fulvus), however, are the exception to the female-dominant pattern in that they show a complex non-linear, non-gender based dominance hierarchy in which few agonistic interactions can be easily interpreted as won or lost. It has been suggested that this lack of female dominance is related to the relative non-monopolizability of the folivorous diet of this species, although this is not supported by recent field observations which show this species as significantly frugivorous. Our research has first focused on the ecological basis of the non-female dominant social system of this species, and has then expanded to include a multi-species, multi-level study of the evolution of aggression-based dominance and non-aggression based “power” in primates.

In contrast to our results with ring-tailed lemurs, our feeding trials with brown lemurs (Eulemur fulvus) at the Duke University Primate Center show no effect of increased feeding competition on the expression of female dominance or even within-group aggression. Instead, we found that aggression is directed primarily out of the group, in this case at another species. As has been observed in field studies, we also determined that brown lemur males serve as aggressive partners for individual females during feeding. We have also found from studies in the wild that brown lemurs are the most successful inter-specific competitor and can oust even larger ruffed lemurs from food patches with their cooperative strategy of inter-specific competition. There are also frequent inter-group interactions with other brown lemurs. These results have led us to examine the hypothesis that brown lemur agonistic behavior is a strategy for inter-specific competition and/or inter-group competition.

Despite the lack of relationship between feeding competition and social dominance, we found that females were generally able to obtain feeding priority without aggressive social interactions. Dominance in human and non-primates can be divided into two main areas: aggressive dominance, as reflected by the consistent asymmetry in outcomes of aggressive conflicts, and control of power, as in the control of food or other important resources. Our studies suggest that brown lemur females may be exercising power within their groups in a way that has not been detected by more traditional methods of measuring and classifying animal behavior.

These results, as well as those from our studies of Lemur catta, have led to an expansion of our research to a multi-species, multi-level study on the evolution of aggression-based dominance and non-aggression based “power”.