Wednesday, October 14, 2009

Figure 2 from Lahdenperä et al. (2004)

FIGURE 2. Post-reproductive mother presence (at the time that each offspring began to reproduce) and correlates of each offspring's (son and daughter) fitness and key life-history traits in Finland.

a–c, Offspring fitness; d–f, Key life-history traits. A living post-reproductive mother is associated with: a, increased lifetime fecundity of offspring (F1,607 = 9.44, P = 0.0022); b, increased lifetime reproductive success of offspring (LRS) (F1,593 = 8.23, P = 0.0043); c, increased numbers of grandchildren produced when post-reproductive mother was living in the same village versus elsewhere (F1,293 = 3.98, P = 0.047); d, reduced ages at first reproduction of offspring (F1,814 = 52.65, P < 0.0001); e, reduced first three inter-birth intervals (F1,977 = 6.45, P = 0.011), but not those thereafter (F1,711 = 0.84, P = 0.36); and f, increased survival of grandchildren until age 15 (log-rank test: 22 = 19.78, P < 0.0001). Panels a–e show predicted means (1 s.e.) from GLMMs after controlling for effects of offspring socio-economic status, geographic and temporal differences in living conditions, birth order, sex, number of siblings, mother's age and repeated measures of mother, where appropriate. Panel f shows Kaplan–Meier survival curves for grandchildren depending on the age and presence of a post-reproductive grandmother.

Saturday, August 18, 2007

Chimpanzees and Bonobos: More Similar Than We Thought?

Review of Behavioural Diversity in Chimpanzees and Bonobos edited by
Christophe Boesch, Gottfried Hohmann, and Linda F. Marchant. Cambridge,
Cambridge University Press, 2002

Rybak, J. 2004. American Journal of Primatology 63:245–249

This comprehensive work on the study of behavioral diversity in wild populations of chimpanzees and bonobos (Pan) is based largely on the proceedings of a conference entitled “Behavioural Diversity in Chimpanzees and Bonobos,” which was held in June 2000 in Seeon, Germany. The conference was organized and hosted by the editors of the book, and included presentations by 30 invited international scientists studying 13 different wild populations of Pan paniscus (bonobos) and Pan troglodytes (chimpanzees). Although it is based heavily on contributions from the conference, the book also contains chapters from other researchers in the field. Taken together, these studies address a broad range of behavioral diversity both within and between wild populations of Pan, and do justice to the book’s seemingly ambitious title.

The overall goal of the book is to document and assess the most current knowledge regarding behavioral diversity in wild populations of Pan by focusing on both species-typical and population-typical behavior patterns. A large body of literature already exists on the topics discussed in the book. Nevertheless, this book provides new and exciting information that supplements the current data. Additional data from ongoing longitudinal studies and from lesser-studied populations of both species are examined. Areas where further research is required are also highlighted, indicating promising new avenues of study. The book includes 19 articles, which are presented in five main sections: Behavioural Diversity, Social Relations, Female Strategies, Hunting and Food Sharing, and Genetic Diversity.

In the first section, Chapter 1 (by Doran et al.) encompasses what I find to be the most interesting part of the book. In the process of identifying the variability among chimpanzee and bonobo populations, it becomes clear that the distinction between the two species is not as clear-cut as previously thought. While certain species distinctions still hold true, such as female- vs. male-dominated societies, and differences in tool use, other distinctions are brought into question. This is largely because the taxonomic grouping of these two species has been based on incomplete behavioral data. However, the data presented in this section illustrate that as we learn more about population-specific differences within each species, the distinction between the species becomes more blurred. For instance, while Mahale and Gombe chimpanzees are taxonomically similar, and Wamba and Lomako bonobos are similar, the chimpanzee populations of Bossou and Tai forest vary in their placement along the taxonomic spread. As an additional example of these behavioral distinctions exemplified throughout the book, Matsumoto-Oda (Chapter 12) suggests that “the gregariousness seen at Mahale might not be characteristic of chimpanzees in general” (p. 177). Since a great deal of our understanding of these species is based on a few specific groups, it seems that the full breadth of Pan behavior is not yet well understood. Thus, it becomes obvious to the reader that it is difficult to say whether or not chimpanzees and/or bonobos have specific behavioral repertoires, a theme present throughout the remainder of the book.

In Chapter 2, Hunt and McGrew provide further evidence for this theme by drawing on observations of wild savannah chimpanzee populations at Assirik, Senegal, and Semliki Wildlife Reserve, Uganda. The habitats of these populations are quite different from those of forest-dwelling groups, such as the Gombe and Mahale groups in Tanzania. Ecological differences between the savannah sites and Tanzania, including forest structure and predation pressure, result in a range of different behaviors. The savannah chimpanzees nest in larger groups, possibly due to predation pressure, and range farther than other populations of chimpanzees, possibly due to the limited forest canopy. In addition, preferences for prey items and hunting styles are different between forest- and savannah-dwelling chimpanzees. In contrast to forest-dwelling chimpanzees, the Semliki population rarely hunts, and no carnivory has been observed. Chimpanzees at Assirik consume two species of nocturnal prosimian (Galago senegalensis and Perodicticus potto) instead of the preferred red colobus (Procolobus badius) hunted by chimpanzees in Tanzania. Rather than actively pursuing prey, as east African chimpanzees do (see Boesch et al., Chapter 16), the chimpanzees of Assirik take prosimians from nesting areas and sleeping holes during the day.

Throughout the book are examples of behaviors seen only in certain populations of chimpanzees and bonobos, such as tuber-eating by chimpanzees in Tongo (Chapter 3), where water is sometimes scarce and the animals have adapted accordingly, and the grooming hand-clasp that is observed in only a few populations of chimpanzees (Chapter 5). Examples such as these, initially presented as outliers of ‘‘typical’’ chimpanzee behavior, are now being used to broaden our understanding of the diversity of the species. Rather than simply describing these differences among populations, the authors have attempted to explain them in terms of ecological and evolutionary variations (e.g., Chapter 5 by Nakamura).

The second section of the book investigates social relations within various populations of chimpanzees and bonobos. Party composition in chimpanzees is addressed by the first two chapters of the section (Chapter 6 by Anderson et al., and Chapter 7 by Mitani et al.), which are somewhat confusing. In reading Chapter 7, it seemed to me that the information presented was slightly redundant, since it covered many of the same points discussed in the previous chapter. Indeed, both chapters investigate essentially the same topic in two different populations of chimpanzees, focusing on party size, estrous females, and food abundance. However, neither provided the cohesiveness that might have been better accomplished by combining efforts. In addition, the work of Wallis in Chapter 13 provides further data related to this topic, which suggest that seasonality and food abundance influence the estrous cycle of females. Since Chapters 6 and 7 addressed estrous females and food abundance as factors affecting party size, the addition of data from Wallis’s study might have provided a more complete understanding of chimpanzee social dynamics while combining studies from four chimpanzee sites (Tai (Chapter 6), Ngogo (Chapter 7), and Gombe and Budongo (Chapter 13)).

Male chimpanzee relationships in Budongo Forest are examined by Newton-Fisher in Chapter 9. Data were collected regarding the association and proximity of male chimpanzees during a period when their social relations were unstable and a change in alpha status occurred. While the results did not indicate that changes in social status had an effect on the grooming, association, and proximity of the males, the author postulates that the differences were not seen because the shift in status was beginning to take place prior to the onset of the study. Therefore, collecting data over a longer time period may help complete the picture of adult male chimpanzee associations throughout the course of status changes. However, the results did indicate that “for individual males, the size of the party may be less important than the number of other males, and the number of males may be less important than the identities of those other males’’ (p. 135).

Studies such as these may also provide useful information in terms of the welfare and management of captive populations, some of which include bachelor groups. The social organization of bonobos as presented by Hohmann and Fruth (Chapter 10) provides not only an interesting comparison with chimpanzee society, but also new information about bonobos. This study investigates the effect of estrous females and food abundance on the social organization of bonobos (similarly to the first two chapters of the second section), in addition to exploring intercommunity contacts. This chapter also provides support for the overall theme of the book, in that bonobos are similar to the chimpanzees of Tai forest in terms of party size and patterns of association, and share a similar habitat. In fact, the authors make the bold statement that in their opinion, “the behavioral diversity of bonobos resembles that of chimpanzees” (p. 147), a statement that is well supported by their research.

The third section of the book discusses female social and sexual strategies. In this section the commonly-held view that bonobos are the more sexually active of the two species is challenged. Furuichi and Hashimoto (Chapter 11) found that the rate of copulation for estrous females was actually lower in bonobos than in chimpanzees. The authors do a superb job of examining various hypotheses to explain these findings, and discuss many of the implications and strategies that are associated with differences in sexual behaviors. Nevertheless, the notion that bonobos are more sexually active than chimpanzees may still be valid if noncopulatory sexual behaviors or those occurring outside the estrous period are included. Furthermore, since this chapter compares the bonobo data primarily to previous data on eastern chimpanzees, the inclusion of data from western chimpanzee populations may reduce the clear distinctions seen in this chapter.

Wrangham continues the underlying theme of the book by examining the sexual attractiveness of chimpanzees and bonobos in Chapter 15. By including new data from east African chimpanzees, Wrangham applies his cost-of-sexual-attraction hypothesis to numerous populations of Pan in order to illustrate differences in such factors as the copulation rate, number of mating days per conception, and male coercion and mate guarding. These differences are evaluated with ecological and demographic factors in mind.

Hunting and food-sharing are the common themes in the fourth section. This section is especially interesting because Fruth and Hohmann test several hypotheses to explain food-sharing in bonobos (Chapter 17). Similar hypotheses could be inferred in the next chapter from the data presented by Watts and Mitani on chimpanzee hunting and food-sharing. While Fruth and Hohmann found that bonobos share food based on mutualism and buy-off strategies, Watts and Mitani report that chimpanzees share meat based on what appears to be reciprocity. One of the most interesting disparities between chimpanzee and bonobo hunting is that bonobos successfully hunt alone. This may be because bonobos prefer to hunt species such as duikers (Cephalophus spp.), a solitary, ground-dwelling ungulate, or forage for large fruits such as Treculia africana and Anonidium mannii, while chimpanzees prefer to hunt red colobus (Procolobus badius), a highly active, group-living, arboreal species, which requires a certain level of cooperation. A combined study on food-sharing and hunting behaviors among various Pan populations, or a chimpanzee study designed in a manner similar to that used by Fruth and Hohmann could potentially clarify the behavioral differences between the species. As an interesting aside, it was found that female bonobos do not share food with males who are being aggressive (Chapter 17), whereas aggression appears to be an important part of chimpanzee life (although it was not considered in Chapter 18 as a variable in whether or not one received food from a possessor). Since bonobos are commonly thought to be the more peaceful of the Pan species, is it possible that the females are in a sense training the males to be less aggressive by not reinforcing their behaviors?

While I read these chapters, the thought of a child throwing a tantrum in a candy store and being reinforced by an exasperated mother came to mind. The child, being reinforced by getting what he wanted, would likely continue to throw tantrums in the future in order to get candy from his mother. This basic training concept of extinction (bonobos) vs. variable reinforcement (chimpanzees) may be a feasible explanation for some of the differences in aggressive behaviors observed in Pan.

In Chapter 16, Boesch picks up the common thread of behavioral diversity in terms of predator–prey relationships among different populations of chimpanzees. The finding of stark contrasts in hunting styles (for example, quietly assessing the situation vs. actively hunting) exemplify the behavioral diversity found among populations of chimpanzees. These differences are again explained in terms of ecological and demographic differences.

The final section of the book, Genetic Diversity, is covered exclusively by Bradley and Vigilant in the final chapter. The authors provide a thorough review of the current knowledge regarding chimpanzee and bonobo genetics. They discuss the general methods of molecular analysis, and approach genetic diversity and similarities through phylogeny, systematics, and socioecology. While the chapter is heavy with terminology, the authors provide a detailed summary of the current understanding in this emerging field, supplementing the behavioral research presented in the preceding chapters. The addition of genetic information to behavioral and morphological data assists in the completion of a comprehensive understanding of the diversity of these species.

Overall, I found this book to be a useful supplement to my own knowledge and experience gained from working with chimpanzees. I believe this book makes an important contribution to the field of primatology, and will be of great interest to both students and researchers from a wide range of backgrounds, such as primatology, ecology, anthropology, ethology, and comparative psychology. In addition, those who care for these animals in sanctuaries and captivity will benefit from a more complete picture of the natural behavioral diversity of the animals in their charge. The work presented in this book is also essential to the conservation of these species. The data presented clearly indicate that we still have much to learn about the behavioral diversity among the populations and between the species of Pan, and that this diversity exceeds previous estimates that were based on just a few groups. I look forward to continued information generated from each of the populations being studied, and highly recommend this book to anyone interested in chimpanzee and bonobo behavior.

Jennifer L. Rybak
Yerkes National Primate Research Center
Emory University
Lawrenceville, Georgia

The Ten Punishments

Let's post these in the schoolroom!

From Positive Atheism

1. Exodus 22:20: He that sacrificeth unto any god, save unto the Lord only, he shall be utterly destroyed.

2. Leviticus 24:16: And he that blasphemeth the name of the Lord, he shall surely be put to death.

3. Exodus 31:15: Whosoever doeth any work in the Sabbath day, he shall surely be put to death.

4. Exodus 21:15: He that smiteth his father, or his mother, shall be surely put to death.

5. Exodus 21:17: He that curseth his father or his mother, shall surely be put to death.

6. Exodus 22:19: Whosoever lieth with a beast shall surely be put to death.

7. Leviticus 20:13: If a man lie with mankind, as he lieth with a woman, both of them have committed an abomination: they shall surely be put to death.

8. Leviticus 20:10: And the man that committeth adultery with another man's wife, the adulterer and the adulteress shall be put to death.

9. Mark 16:16: He that believeth not, shall be damned.

10. Malachi 2:1-4: And now, O ye priests, this commandment is for you. If you will not hear, and if ye will not lay it to heart to give glory to my name, ... behold, I will corrupt your seed, and spread dung upon your faces.

Sunday, August 5, 2007


The Primate Diaries is a personal blog and will not discuss my professional or academic work.

The views and opinions expressed on The Primate Diaries are purely those of the author and should in no way reflect the views or opinions of his university, his department, the sources he cites, any of the writers this page links to, his friends and relatives, his church group or his species.

Saturday, August 4, 2007

Spite: Evolution Finally Gets Nasty

Altruism's "neglected ugly sister" comes to the party
The Scientist 2004, 18(24):14
By Stuart Blackman

The body of a caterpillar is the site of both a great feast and a gruesome familial struggle. But unlike even the most dys-functional holiday dinners, this fight for food erupts into bloodbath, with sisters killing sisters and brothers alike. The slaughter, as damaging to killer as to killed, exemplifies an ugly facet of evolution – the role of spite.

Partaking in this grisly feast are the larvae of a parasitoid wasp, Copidosoma floridanum. Like other wasps, Copidosoma are haplodiploid: Fertilized eggs produce females; unfertilized eggs become males. These wasps are also polyembryonic: Eggs split to produce many clonal embryos. A single host may contain multiple eggs from multiple females, resulting in a hodgepodge of genetic relationships. The violence erupts when a proportion of the larvae (mostly females) develop into sterile soldiers armed with large mandibles, whose sole purpose is to seek out and kill less-related larvae.

"They're more nasty to sisters than they are to clonal sisters. They're even more nasty to brothers, and they're really nasty to ones that aren't genealogically related," says Stuart West, research fellow at the University of Edinburgh.

Sterile castes are well known among the social insects. The majority of ant workers, for example, altruistically forego reproduction to serve their queen. But according to West, the murderous Copidosoma soldiers are not altruists, even though their closest kin will benefit from the slaughter. "They're not preferentially helping someone else; they're preferentially killing someone else," says West, and that's a whole different class of behavior.1

Spite, the "neglected ugly sister of altruism,"2 is undergoing something of a renaissance. Theoretical developments suggest that spite is more widespread in nature than believed. Some researchers think spite might shed light on the ecology and evolution of disease virulence, informing intervention strategies against pathogenic infections.


Social behavior is organized conventionally into four classes, characterized by the costs and benefits to actors and recipients. Selfishness and mutualism are relatively straightforward: The actor benefits from its own behavior. Altruism and spite, in which the actor's fitness is impaired by its actions, have proven more problematic. Not until the 1960s did Oxford's Bill Hamilton show that genes for altruism can boost an individual's inclusive fitness, proliferating in the relatives that benefit, provided that the advantage to the recipient multiplied by its coefficient of relatedness to the actor (0.5 for full siblings, 0.25 for nephews, etc.) is greater than the cost incurred.3

Hamilton also recognized spite as a theoretical possibility, if the recipient is negatively related to the actor, that is, less related than a random member of the population.4 But he also recognized an important difference with altruism: When a spiteful actor removes a negatively-related recipient, all the remaining individuals benefit, not just the actor's kin. Selection for spite is, therefore, relatively weak.

Harvard University's E.O. Wilson offered a solution by suggesting that spite could be favored without negative relatedness if the act also specifically benefits positively related individuals.5 While nature seemed rife with examples of altruism, however, spite was elusive. "It got to the stage in the literature where people were saying there are no examples of spite at all," says Kevin Foster of Berlin's Institute for Advanced Studies. "So we went back to the original definitions and tried to work out where they applied."

Foster identified three cases of spite among social insects.6 The first, worker policing, is widespread among ants, bees, and wasps. Workers invest time and energy to kill the male offspring (the actors' nephews) produced by rogue workers. In the second case, the Argentine ant (among others) displays sex allocation biasing; workers kill brothers to shift the colony sex ratio in favor of females. And in a unique third case, red fire ant workers kill queens that do not share an allele at a particular locus (Gp-9). Foster interprets these as Wilsonian spite, because they indirectly benefit a more closely related third party: respectively, brothers, sisters, and queens, with the same Gp-9 allele. But he also considers the fire ant example to have a Hamiltonian flavor, in that the spiteful Gp-9 allele is negatively related to that of the victim.

"[Hamilton] saw it as very hard to get situations where you could get appreciable negative relatedness," says West. "He argued that that needed really small population sizes." But West says that negative relatedness can arise if competition for resources is highly localized.2


In the closed world of a fig, for example, where male fig wasps compete intensely for access to a limited number of females, males are as aggressive towards brothers as towards unrelated males. "There's no point helping one brother if the extra benefit they get comes at the cost of another brother," says West. So, for social interactions, relatedness is not absolute; it is relative, depending on who the competition is.

When West's doctoral student, Andy Gardner, applied standard fitness equations to social behavior under local competition, what popped out at the end was Hamilton's rule with a negative relatedness and a negative benefit: Hamiltonian spite. "We haven't put negative relatedness into the analysis," says Gardner. "That's something that falls out naturally."

So, in the case of Copidosoma, larvae compete for resources within a caterpillar host, not with the global wasp population. Average relatedness between competitors is zero, so the presence of clonal siblings indicates significant negative relatedness between other individuals, and even between nonclonal relatives. Foster says that in taking scale of competition into account, his examples of Wilsonian spite become Hamiltonian. "Everything [West and colleagues] say stands, so long as it's OK to change the scale at which you measure relatedness."

But not everyone says it's OK. "Yes, competition is occurring on a very local scale within generations," says Michael Strand, a professor of entomology who works on Copidosoma at the University of Georgia, Athens. But the larvae will eventually disperse as adults when "there's plenty of opportunity for mixing between individuals of different generations," Strand says. West maintains that the scale of competition to consider is that which encompasses the trait being studied. Nevertheless, for the moment, Strand prefers to view the murderous soldiers as "indirect altruists."


Strand says he finds another putative spiteful system "more compelling." Many bacteria manufacture toxins called bacteriocins, which they release explosively, killing both themselves and sensitive competitors, but sparing clonal relatives that possess a resistance gene. Gardner says the spiteful credentials of such bacterial suicide bombings are reinforced by the presence of an equivalent altruistic trait, siderophore production. Siderophores are compounds that scavenge iron from the environment for absorption. "You do better as a bacterium if you don't produce the proteins and just mop up those produced by others. So, production of the proteins is altruistic," says Gardner. In line with predictions, West's team, in collaboration with Angus Buckling at Oxford University, has shown that bacteriocin production is increasingly favored by selection, as competition between bacterial strains becomes more local,7 whereas siderophore output declines.8

Such microbial social dynamics could illuminate understanding of virulence. The prevailing view, says West, is that high kinship between parasites selects for prudent exploitation of a host and, therefore, lower virulence. But with siderophore production, says West, "They cooperate more and that makes them nastier." Spite provides a third scenario: Buckling has shown that chemical warfare between spiteful bacterial genotypes reduces virulence.

Buckling says the findings are particularly relevant if antibiotic use encourages clonal expansions of bacteria. "We would expect bacteriocin production to go down and virulence [to] go up, because these bugs are not killing each other, and they're not investing into producing bacteriocins." Adds West, "If you can think up ways to make bacteria more spiteful to each other, they'd be less effective at growing in the host."

The parallels between the bacteriocin system and human suicide-bombings are striking, at least superficially. West says that, whether biologically or culturally driven, human social strategies can be influenced by competitive scale. He describes an experiment in which undergrads played prisoner's dilemma (a classic game used to explore cooperative strategies) in five groups of three. For global competition, the top five scores won cash prizes; for local competition, prizes went to the top scorer in each group. "They were much less cooperative when they competed locally," he says.

Whether such approaches can advance understanding in human social behavior is another matter. Nevertheless, Buckling doesn't rule out the influence of competitive scale in his relationship with Edinburgh collaborators. "If we're the only ones working on it," he jokes, "it could get nasty."


1. A Gardner, SA West "Spite among siblings," Science 305: 1413-4. [Publisher Full Text]
Sept. 3, 2004

2. A Gardner, SA West "Spite and the scale of competition," J Evol Biol 17: 1195-203.
[Publisher Full Text] Nov. 6, 2004

3. WD Hamilton "The genetical evolution of social behaviour, I & II," J Theor Biol 1964, 7:
1-52. [PubMed Abstract] [Publisher Full Text]

4. WD Hamilton "Selfish and spiteful behaviour in an evolutionary
model," Nature 1970, 228: 1218-20. [PubMed Abstract]

5. EO Wilson Sociobiology: The New Synthesis Cambridge, Mass.: Harvard University
Press 1975.,

6. KR Foster et al, "Spite: Hamilton's unproven theory," Acta Zool Fennici 2001, 38: 229- 38.

7. A Gardner et al, "Bacteriocins, spite and virulence," Proc R Soc Lond B 271: 1529-35. July 22, 2004

8. A Griffin et al, "Cooperation and competition in pathogenic bacteria," Nature 430: 1024- 7. [Publisher Full Text] Aug. 26, 2004