john hawks weblog

paleoanthropology, genetics and evolution

chimpanzees

  • Great apes and human diseases: how primatologists hurt and help

    Fri, 2008-02-29 15:23 -- John Hawks

    A new paper in Current Biology documents the mortality suffered by Taï Forest chimpanzees as a result of common human respiratory ailments during the last ten years. Tissue samples of deceased animals provided information about the pathogens that caused the outbreaks:

    Necropsy samples were screened for respiratory pathogens by using different PCR methods. As for most human respiratory cases, a mix of bacterial and viral respiratory pathogens was found in the lungs. The most common bacterium was Streptococcus pneumoniae, which was found in all respiratory outbreaks. In addition, Pasteurella multocida played a role in the 2004 outbreak [10]. All available samples tested positive for one of two paramyxoviruses: human respiratory syncytial virus (HRSV) was diagnosed in two individuals that died in the 1999 north group outbreak and in one adult female (east group) and one infant (south group) who died in the 2006 outbreak, which occurred simultaneously in both groups. The second virus identified was human metapneumovirus (HMPV), detected in three animals that died in the 2004 south group outbreak (Table 1).

    Humans have suffered from these respiratory ailments for a long time. The number of human respiratory pathogens almost certainly proliferated greatly during the last 10,000 years, after the advent of agriculture and village life brought the potential of "crowd diseases." For example, human respiratory syncytal virus (HRSV) is closely related to the bovine BRSV and pneumonia virus of mice (PVM). It seems plausible that the human pathogen descended from the mouse or cattle (or sheep) virus, but no one has yet demonstrated this -- and it is after all possible that they got it from us. HRSV is an important cause of lower respiratory tract infections in humans worldwide, especially in children. In an ironic twist, HRSV was first identified in captive chimpanzees as the cause of a respiratory infection with runny nose and sneezing (called coryza) (Blount et al. 1956). It was actually the human RSV virus contracted by the chimpanzees that had caused the infections.

    Much the same thing has happened to the wild chimpanzees, but with a high death toll. A 1999 outbreak of HRSV, compounded by Streptococcus pneumoniae, killed 6 out of 32 animals in the affected group, including 5 adults. A 2004 outbreak killed 8 out of 44 animals. These two outbreaks each killed nearly a fifth of the chimpanzees in these groups, and demographic records show that several "multiple mortality events" in the last 24 years are not attributable to poaching or other diseases such as ebola or anthrax (each of which had least one outbreak).

    Easily spread respiratory ailments are among the main causes of sickness in contemporary hunter-gatherers, partly because they are able to persist and spread effectively in low-density populations, and partly because they are so common in neighboring groups. Today, respiratory diseases are an important cause of death in these groups -- including adults -- although they count for fewer deaths than gastrointestinal pathogens and parasites. Their ability to infect low-density populations suggests that some human respiratory pathogens surely date to much earlier periods of human evolution.

    One thing is certain: humans have undergone thousands of years of selection, in which susceptible individuals have disproportionately been killed by human-infecting respiratory viruses and bacterial strains. Many of these pathogens have adapted very well to humans, including a substantial time or fraction of the population in which they may be present without causing noticeable symptoms.

    Chimpanzees lack this history. Relatively minor diseases in humans may have major effects on chimpanzees, and diseases like RSV that cause measurable mortality among human infants may have devastating effects on chimpanzee communities. Together, respiratory illnesses, ebola, and anthrax are having a death toll in the studied chimpanzee groups almost as great as smallpox in post-contact American Indians.

    The shocking thing is that this enormous death toll seems likely to have been caused by the researchers themselves, along with ecotourists:

    It has long been recognized that respiratory disease is the most important cause of morbidity and mortality among wild great apes habituated to human presence for research or tourism [4], [24], [25], [26] and [27]. However, the etiological agents of such disease have not been documented. Possibly as a consequence of respiratory disease, about half of the long-term chimpanzee research populations have shown major declines [4] and [28]. Our results suggest that the close approach of humans to apes, which is central to both research and tourism programs, represents a serious threat to wild apes (Köndgen et al. 2008:262).

    The authors temper this conclusion in two ways. First, they show that the presence of the research station and the tourist site both have significantly decreased the incidence of poaching at and around these areas. Both areas have lots of chimpanzees, but little sign of poachers in contrast to the rest of the protected forest, where poacher sign is common. Poaching accounts for nearly as many documented deaths in the study population as respiratory infection, so this protective effect may be very important.

    On the other hand, communicable diseases may well spread beyond a single group, so much of the forest may be at high risk from both poaching and human pathogens. And needless to say, poachers may spend less time around the research and tourist areas, but that hasn't stopped them from killing lots of chimpanzees there. So the protective effect may not be much of a shield.

    Second, they provide recommendations that may decrease the risk to the chimpanzees while permitting continued human presence:

    In order to reduce the negative effects of research and tourism, strict hygiene protocols, including vaccination requirements for tourists, tourism personnel, park staff, and research personnel against all potentially dangerous diseases for which vaccines are available (e.g., measles, mumps, and rubella), should be implemented [5], [6], [29] and [30]. Only nonsymptomatic visitors and staff should have access to habituated apes. Feces, vomit, and other human debris or wastes should be removed from areas where chimpanzees may come in contact with it or buried at a depth where other animals will not uncover it [29]. Because carriers of human respiratory pathogens are often nonsymptomatic, wearing of masks (e.g., N95 masks as recommended for avian flu) [31] should be mandatory. Human populations living around the parks and reserves should be vaccinated, thereby decreasing the chances of human-pathogen introduction into chimpanzee populations. As in the Taï project, demographic, clinical, and diagnostic monitoring systems should be implemented to objectively document the negative effects of research or tourism. Furthermore, we urge an intensification of research on ways to prevent disease transmission, as well as the development of new methods for vaccine and treatment delivery, to wild apes (e.g., oral baiting) (Köndgen et al. 2008:262-263).

    These are necessary precautions, but they are unlikely to be enough. There is no effective or widely available for RSV, or HMPV. S. pneumoniae normally exists in the respiratory tract of 10 percent of healthy adults. There is no way that chimpanzees can hold off these diseases if they are in recurrent contact with people.

    References:

    Blount RE Jr, Morris JA, Savage RE. 1956. Recovery of cytopathogenic agent from chimpanzees with coryza. Proc Soc Exp Biol Med 92:544-549.

    Köndgen S and 17 others. 2008. Pandemic human viruses cause decline of endangered great apes. Curr Biol 18:260-264. doi:10.1016/j.cub.2008.01.012

    Tags: 
    conservation
    disease
    chimpanzees

  • Broca's area and chimpanzee communication

    Thu, 2008-02-28 23:45 -- John Hawks

    Chimpanzees use their own version of Broca's area when they communicate, according to a new PET scan study by Jared Taglialatela and colleagues. The abstract:

    Broca's area, a cerebral cortical area located in the inferior frontal gyrus (IFG) of the human brain, has been identified as one of several critical regions associated with the motor planning and execution of language. Anatomically, Broca's area is most often larger in the left hemisphere, and functional imaging studies in humans indicate significant left-lateralized patterns of activation during language-related tasks [1], [2] and [3]. If, and to what extent, nonhuman primates, particularly chimpanzees, possess a homologous region that is involved in the production of their own communicative signals remains unknown. Here, we show that portions of the IFG as well as other cortical and subcortical regions in chimpanzees are active during the production of communicative signals. These findings are the first to provide direct evidence of the neuroanatomical structures associated with the production of communicative behaviors in chimpanzees. Significant activation in the left IFG in conjunction with other cortical and subcortical brain areas during the production of communicative signals in chimpanzees suggests that the neurological substrates underlying language production in the human brain may have been present in the common ancestor of humans and chimpanzees.

    I wrote a couple of years ago about the Broca's area homolog in macaques, and the involvement of the area in planning time-sensitive action sequences in people. Those studies clearly foreshadowed the current result, since they provide both a phylogenetic expectation that this brain area evolved early in anthropoid evolution (or earlier), and the functional expectation that motor sequences characteristic of communication depend on it.

    There is some uncertainty in the current analysis, because the PET scanning method doesn't localize the increased activity as tightly as they would like:

    Although these data indicate that the left IFG is involved in the production of communicative signals in chimpanzees, cytoarchitectonically, it is not clear what cell types fully comprise this region [36]. Therefore, it is not possible to determine whether or not the neuronal metabolic activity reported in this study corresponds to an area within the chimpanzee IFG that contains Brodmann's area 44/45 cells -- those cells that comprise Broca's area in humans. In fact, additional areas of significant activation are observed in the frontal orbital gyrus and the frontal pole (Figure 2). Additional work is needed to explore the significance of these areas of activation.

    Nice piece of work. I wouldn't want to be the one to get a chimp into a scanner...

    References:

    Taglialatela JP, Russell JL, Schaeffer JA, Hopkins WD. 2008. Communicative signaling activates 'Broca's' homolog in chimpanzees. Curr Biol 18:1-6. doi:10.1016/j.cub.2008.01.049

    Tags: 
    communication
    chimpanzees

  • Fongoli chimpanzees, Pruetz profile

    Wed, 2008-02-27 08:02 -- John Hawks

    National Geographic sent writer Mary Roach to see the Fongoli chimpanzees, at the field site of primatologist Jill Pruetz. The result is a nice story about the difficulties of establishing and running a field site, and the joys of watching chimpanzees do things no one has ever seen before.

    Now here comes Farafa, her baby Fanta on her back and a bushbuck haunch in her jaws. It's a complicated, messy piece of anatomy, with sinew and hide hanging off one end. Tia sees her and stands up to move away. My last glimpse of Tia is with her now bare bone brandished above her head, standing erect, as though reenacting the "dawn of man" scene from 2001: A Space Odyssey.

    Fongoli chimps have a flair for the dramatic.

    It's a funny thing about the range of a set of observations: New observations can only increase it, never decrease it. People tend to forget that, as long as we are considering the range of behaviors, studying chimpanzees can do nothing but make them overlap with humans more and more.

    The Fongoli chimpanzees are in Senegal, at the very western limit of the chimpanzees' range. Their savanna-woodland territory may be the reason for many of their unique behavior patterns, really the impetus for the article. Roach describes a conservation scenario somewhat different than that in much of the current chimpanzee habitat in other parts of Africa:

    [T]he animals are accorded a remarkable amount of respect by locals. Kerri Clavette, Pruetz's intern, interviewed villagers about their beliefs regarding chimpanzees and whether they hunted them. Among the region's main tribes -- the Malinke, Bedik, Bassari, and Jahanka -- chimps, compared with monkeys, have an elevated, almost human status. "Chimpanzees came from man, as they have similar hearts," a villager told Clavette. Behaviors normally associated with a baser nature -- such as walking on all fours -- were given a respectful spin: "Chimpanzees walk on their knuckles to keep their hands clean to eat with." Chimpanzee origin myths feature humans running off into the woods for some reason -- war, fear of circumcision, fear of being punished for fishing on Saturday -- and staying there so long that they turn into chimpanzees.

    The article includes several anecdotes about the culture of male chimpanzee researchers (that is to say, male researchers of chimpanzees!) and their reluctance to accept certain female behaviors (such as bushbaby skewering) as much like the male counterparts (such as colobus hunting). I think this is to some extent overblown. The literature has made plain for some time that females are the major transmitters of cultural traits in chimpanzees, and so it would be quite silly to deny the importance of females in bearing such traits in the first place. The dispute over the meaning of hunting is mostly semantic -- the real disagreement being whether the motivation for the behavior is food sharing or purely individual foraging.

    And as for the dispute over the meaning of the word, "spear," this really seems to indicate the insularity of certain chimpanzee researchers. Sharpened thrusting weapons were the only such implements available for all but the last 80,000 years or so of human evolution. If we don't call such things, "spears," then a lot of archaeologists are going to be confused!

    Anyway, it's a great article.

    Tags: 
    chimpanzees

  • The antimalarial properties of chimpanzee geophagy

    Mon, 2008-01-14 00:19 -- John Hawks

    It's hard to improve on the headline of this story:

    Why chimps eat dirt

    ...

    [Sabrina] Krief collected the dirt along with leaves from one of the chimps' favorite foods, the Trichilia rubescens plant. She found that when eaten alone, the leaves had no pharmacological effect, but when combined with soil, the mixture had clear anti-malarial properties.

    Scientists previously suspected that animals might eat dirt when stressed or as a source of missing minerals. This new result is the first suggestion that the combination of soil and other foods could have health benefits, Krief said.

    The story also discusses the use of high-kaolinite dirts as antidiarrheal treatments in local peoples -- kaolinite being the nameworthy ingredient of Kaopectate, although it is no longer used in that medication.

    Anyway, this is a good excuse to use the word "geophagy." Great word.

    Tags: 
    chimpanzees
    diet

  • Did Gen Suwa just save paleoanthropology?

    Thu, 2007-08-23 08:21 -- John Hawks

    That depends on whether these teeth are really from a gorilla, I suppose.

    Chororapithecus teeth compared to gorilla mandible

    Chororapithecus abyssinicus teeth compared to gorilla mandible. Photo credit: Gen Suwa/University of Tokyo.

    Oh yeah, sure, "saved paleoanthropology" is overdramatic. But what am I supposed to write? Over four years, we have had a series of genomic comparisons narrowing down the age of the human-chimp common ancestor to something like 2/3 the age of Sahelanthropus. I said it was a crisis, and it is: these data sources must agree. Either we have to cast out a bunch of hominids, or we have to wrench the genes by around a factor of two.

    Now, Suwa and colleagues show up with a 10-million-year-old gorilla. A 10-million-year-old gorilla works just fine with 7-million-year-old hominids. It doesn't work at all with a 7-million-year-old human-gorilla common ancestor. So there's no doubt about the centrality of this particular ancient gorilla -- if it is one.

    So far, all the articles I've seen have someone on the record expressing some reluctance to accept the teeth belonged to the gorilla lineage. Reuters has Peter Andrews; Nature has Jay Kelley; National Geographic has Richard Potts.

    Should we be skeptical? Well, there are lots of convergences among Miocene apes. Many of the dental convergences are detailed in our paper about Sahelanthropus, available open-access from PaleoAnthropology. These convergences make it difficult to identify hominids based on the teeth alone. They also make it hard to say that any particular big-toothed, leaf-eating ape is definitely a gorilla. After all, if it eats like a gorilla, why shouldn't it have teeth like a gorilla?

    Suwa and colleagues go to some pains to demonstrate that the dental similarities with gorillas are more than enamel-deep. Their strongest argument is that the tooth morphology exhibits a derived gorilla-like condition well below the surface, at the enamel-dentine junction. That is, while the tooth was forming, the initial growth surface took on a distinctive shape which was then reflected by the form that the growing enamel took.

    The most distinctive features of the Chororapithecus dentition are the derived shearing structures seen in portions of its molars (Fig. 2), despite a generally low cuspal topography (the latter is apparently a primitive retention).

    Examination of internal morphology by micro-computed tomography (micro-CT) demonstrates that these occlusal features were underlain by distinct enamel-dentine junction (EDJ) structure (Fig. 2). In particular, the straight to weakly concave mesial protocone crest seen in the EDJ of CHO-BT 4, -BT 5 and -BT 6 is gorilla-like, and is formed by a mesiobucally located junction of the mesial protocone crest and mesial marginal ridge. Such spatial placements are best considered to be regulated by enamel-knot-related signalling patterns during early morphogenesis [23, 24], and may be one of the underlying causes of the mesiodistally elongate upper molar shape generally characteristic of folivorous primate species. In the lower molars, the most distinctive EDJ topography occurs at the trigonid crest, the structural counterpart that occludes with the upper molar mesial protocone crest. The high trigonid EDJ crest is continuous between the metaconid and protoconid cusp tips (Fig. 2). Because recent experimental and quantitative genetic studies suggest significant degrees of morphogenetic independence between corresponding upper and lower molar structures [25, 26], the presence of a functionally integral inter-jaw pattern of morphological expression, as seen in the Chororapithecus molars, suggests adaptation by natural selection, as opposed to chance emergence of neutral morphological minutia.

    Still, "minutia" is a loaded term. Why shouldn't an ape that evolves the same shear characteristics as a gorilla molar use the same developmental process to achieve them? The more that development of the teeth are constrained by these genes, the more likely it is that different lineages will evolve in parallel.

    Nor is it entirely obvious that Chororapithecus is actually gorilla-like in these characters. The paper compares two ratios involving cusp dimensions measured internally beneath the enamel cap. That's high-tech, but the ratios do not sort out gorillas from chimpanzees, don't sort Chororapithecus from either of those apes or early hominids, and -- even worse -- it's not even clear how these ratios may vary with size. Does Chororapithecus look sort-of like a gorilla on these ratios because it's a sort-of gorilla? Or because it's big? The enamel is relatively thicker than gorillas, like other Miocene apes and orangutans. Clearly the specimen is much less derived than gorillas, but could that be because it isn't a gorilla?

    Well, there's the problem: there's not too much to go on with these teeth. I think Suwa et al. laid out as good a case as there is. A 10-million-year-old gorilla can't be expected to look just like gorillas today. It's not like the teeth look more like something else besides a gorilla. Gorillas really are far more derived in these dental characters than the Chororapithecus dentition, which makes the comparison more difficult. And so, the conclusion of the paper is equivocal:

    The similarities seen between the two genera raise the possibility that Chororapithecus is a Miocene member of the Gorilla clade. Alternatively, with its combination of thick enamel and distinct molar cresting pattern, Chororapithecus may represent a unique adaptation that is convergent with gorillas in molar structure and function. Although the evidence for phylogenetic affinity between Chororapithecus and Gorilla is inconclusive, it may be that the basal members of the gorilla clade shared large tooth size and incipiently enhanced molar shear as a part of an herbivorous diet that accompanied (presumed) larger body size. Chororapithecus may then represent one example of adaptational (and perhaps phyletic) differentiation within that clade.

    I don't know about anybody else, but I don't think this helps us with our little problem very much. Here's what I think: the problem is not so much the 10-million-year-old gorilla, as it is the 17-million-year-old orangutan that it necessitates. Here's the very next paragraph of the paper:

    Acceptance of Chororapithecus as a basal member of the gorilla clade would push back the gorilla species split to >10.5 Myr ago. Because this is a minimum date established from a meagre fossil record, the actual divergence would have predated this by an unknown time gap. From the currently available evidence, we consider that a species split of 20 Myr ago for Pongo, 12 Myr ago for Gorilla, and 9 Myr ago for Pan are all probable estimates (see Supplementary Information). We consider that the early divergence hypothesis is congruent with both fossil and molecular data, and should be further evaluated using both sides of the evidence.

    I think those dates don't really need to be so old. A 10.5-million-year gorilla divergence could easily correspond to a 17-million-year orangutan divergence. Still, for those of us who have gotten used to the idea that Dryopithecus might have something to do with the origin of African apes, this idea might seem a little troubling. So, let's look at the part of the Supporting Information that, well, supports their assertion that all these dates are "congruent":

    The above summarized molecular predictions are in concert with the notion that the Pongo lineage existed in Africa prior hominoid migration to the Eurasian continent, the earliest such opportunity for dispersal (barring significant rafting) being at circa 17 Ma (44). If in fact the Gorilla split was 12 Ma, then the OWM split estimate (33.6-43 Ma) largely predates the earliest known definitive occurrence of catarrhines (Propliopithecus and Aegyptopithecus) (45), and many would consider this to be somewhat outside an acceptable boundary condition. However, it may be indicative of variable molecular rates of evolution across lineages (46, 47), with higher mutation rates in the OWMs (48) (and early hominoids) because of their shorter generation lengths (48, 49) and/or higher metabolic rate in relation to smaller body mass (50).

    Well, that's a tricky bit of argument. We might believe that African apes never left Africa and that all the dryopithecines are therefore on the orangutan line. At least, that makes some biogeographic sense. But it's hard to argue that any of these dates are "congruent" with genetic evidence as we currently understand it. Many of the recent methods don't make any prior assumptions about "calibrated" divergence times like the orangutan-human divergence. Worse, Hobolth et al. (2007) found a human-chimp speciation time of 4 million years even considering an orangutan-human divergence of 18 million years.

    The "shorter generation lengths" explanation doesn't help much -- after all, if we infer that the current great ape lineages existed as early as 20 million years ago, then almost all of the divergence time is occupied by long-generation-length species. Much faster evolution in Old World monkeys should show a strong signal of acceleration in that lineage (with a higher number of derived substitutions), and we don't see it.

    If we believe these interpretations of the genes, a 10-million-year-old gorilla did not exist. Chororapithecus was something else.

    If we believe that Chororapithecus was a gorilla, then these genetic interpretations are simply wrong. And Dryopithecus was on the orangutan lineage. And hominoids diverged from Old World monkeys in the Eocene.

    And Sahelanthropus could have been a hominid.

    References:

    Suwa G, Kono RT, Katoh S, Asfaw B, Beyene Y. 2007. A new species of great ape from the late Miocene epoch in Ethiopia. Nature 448:921-924. doi:10.1038/nature06113

    Hobolth A, Christensen OF, Mailund T, Schierup MH. 2007. Genomic Relationships and Speciation Times of Human, Chimpanzee, and Gorilla Inferred from a Coalescent Hidden Markov Model. PLoS Genet 3(2): e7. doi:10.1371/journal.pgen.0030007

    Tags: 
    gorillas
    Miocene
    Sahelanthropus
    Ethiopia
    chimpanzees
    Chororapithecus
    Africa
    chumans
    Synopsis: 
    The discovery of a gorilla-like primate may demand a recalibration of the molecular clock

  • Bonobo blowback

    Wed, 2007-08-15 13:15 -- John Hawks

    Following on last month's New Yorker article about bonobos (my comments here), Frans de Waal has penned a response (no permanent link yet; this link may stop working after a week or two). De Waal points out what he sees as a political agenda in Ian Parker's article:

    The main message of Parker's piece could of course have been that fieldwork is no picnic, but instead he went for profound revelation: bonobos are not nearly as nice and sexual as they have been made out to be. Given that the bonobo's reputation has been a thorn in the side of homophobes as well as Hobbesians, the right-wing media jumped with delight. The bonobo "myth" could finally be put to rest. Parker's piece was gleefully picked up by The Wall Street Journal and Dinesh D'Souza (yes, the same one who blamed 9/11 on the left), who accused "liberals" of having fashioned the bonobo into their mascot. D'Souza urged them to stick with the donkey.

    This might all have been amusing if it weren't for the fact that these are not just political skirmishes. At issue is what we know. Parker presented his trip as a fact-finding mission that had unearthed revolutionary new insights. His message was that bonobos are killer apes, just like their cousins, the chimpanzees. The animal kingdom remained "red in tooth and claw," as it ought to be.

    I have to say, I don't buy this idea that the New Yorker is sending out right-wing marching orders. Still, de Waal's point is well-taken -- certainly, there are many who want to push the idea that primates are not peaceful gentle creatures, because it confirms their own view of human nature. Certainly, bonobos are a target for such beliefs, since people have a perception of bonobos that is way beyond their real behavior. Up to now, that perception has fit a stereotype of peace-loving hippie primates. As de Waal points out, that stereotype has gotten them attention, increasing the opportunities to research them. But pushing the stereotype always risks that someone will pop the bubble.

    I don't think that Parker's article was very bubble-popping; it was certainly a lot more reasonable than most of the treatments of science in the New Yorker, or Atlantic, or any number of other "thinking" magazines. The shift in the scientific view of bonobos that he describes is genuine. For example, a 2004 book review by Jennifer Rybak includes this passage:

    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 (Figs. 1.2-1.5, p. 23-24). For instance, while Mahale and Gombe chimpanzees are taxonomically similar, and Wamba and Lomako bonobos are similar, the chimpanzee populations of Bossou and Taï 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.

    That's in a review of the 2002 book Behavioural Diversity in Chimpanzees and Bonobos, by Christophe Boesch, Gottfried Hohmann and Linda Marchant. The book's theme is that our perception of bonobo-chimpanzee differences is changing as a result of our greater understanding of behavioral variation in both species. Obviously, this reflects not only changes in our understanding of bonobos but also chimpanzees, as behavioral variation among field sites has become more and more apparent.

    To my mind, the most important point that de Waal makes in his essay is that bonobos don't fit any stereotype -- like any other primate, they are aggressive in some contexts. He notes the ways in which he has argued for a more nuanced view in his publications and books. That will, of course, continue, and the challenge is for anthropologists to make the more nuanced view a feature of their own thinking and teaching.

    References:

    de Waal, F. 2007. Bonobos, left and right: Primate politics heats up again as liberals and conservatives spindoctor science. eSkeptic Aug. 8, 2007.

    Boesch C, Hohmann G, Marchant LF. 2002. Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, Cambridge, UK.

    Rybak J. 2004. Chimpanzees and bonobos: more similar than we thought? Am J Primatol 63:245-249. doi:10.1002/ajp.20055

    Tags: 
    chimpanzees

  • The chimpanzee sex exchange

    Tue, 2007-08-14 10:57 -- John Hawks

    Duffy, Wrangham and Silk describe in a short paper the correlation of male mating success and support for the alpha male in a group of chimpanzees. The finding isn't surprising -- it's been long assumed that subordinate male chimpanzees participate in coalitions to attain mating rewards -- but it's a nice quantification. Helping the alpha male maintain his status had a much larger impact on mating success than rank.

    References:

    Duffy KG, Wrangham RW, Silk JB. 2007. Male chimpanzees exchange political support for mating opportunities. Curr Biol 17:R586-R587. doi:10.1016/j.cub.2007.06.001

    Tags: 
    chimpanzees

  • A bonobo field report

    Tue, 2007-07-31 23:21 -- John Hawks

    A couple of readers have pointed me to an exceptional article in the current New Yorker, in which writer Ian Parker travels with Gottfried Hohmann to Lui Kotal, the field site where he studies partially habituated bonobos.

    Along with a lot of local color, Parker presents a cogent description of the history of bonobo research. His back-and-forth interviews with Hohmann and Frans de Waal illuminate the differences between field and captive primate research, which give rise to a current disagreement about bonobo nature:

    "It was so easy for Frans to charm everyone," Hohmann said of de Waal one afternoon. "He had the big stories. We don't have the big stories. Often, we have to say, 'No, bonobos can be terribly boring. Watch a bonobo and there are days when you don't see anything -- just sleeping and eating and defecating. There's no sex, there's no food-sharing.' " During our first days in camp, the bonobos had been elusive. "Right now, bonobos are not vocalizing," Hohmann said. "They're just there. And if you go to a zoo, if you give them some food, there's a frenzy. It's so different."

    Captivity can have a striking impact on animal behavior. As Craig Stanford, a primatologist at the University of Southern California, recently put it, "Stuck together, bored out of their minds -- what is there to do except eat and have sex?" De Waal has argued that, even if captive bonobo behavior is somewhat skewed, it can still be usefully contrasted with the behavior of captive chimpanzees; he has even written that "only captive studies control for environmental conditions and thereby provide conclusive data on interspecific differences." Stanford's reply is that "different animals respond very differently to captivity."

    Then there is the most powerful bonobo stereotype -- the sex thing:

    When I asked Hohmann about the bonobo sex at Lui Kotal, he said, "It's nothing that really strikes me." Certainly, he and his team observe female "g-g rubbing," which is not seen in chimpanzees, and needs to be explained. "But does it have anything to do with sex?" Hohmann asked. "Probably not. Of course, they use the genitals, but is it erotic behavior or a greeting gesture that is completely detached from sexual behavior?"

    A hug? "A hug can be highly sexual or two leaders meeting at the airport. It's a gesture, nothing else. It depends on the context."

    This is a book chapter-length article, and worth printing out and reading closely. We could use a half-dozen more like it on different primates.

    Meanwhile, if you're interested in reading more about bonobo field research, I can pass along a link to the Lomami blog at Wildlife Direct, where Ashley Vesper writes about his experiences surveying bonobo populations along the Lomami River.

    Tags: 
    chimpanzees

  • The Bili chimpanzees

    Sat, 2007-07-14 20:10 -- John Hawks

    A nice piece in The Guardian about the chimpanzee population near Bili, DRC. The lede is the suspicion of an apparent leopard kill -- that's chimpanzees killing a leopard -- but the other details are interesting:

    [Cleve] Hicks said the animals also have what he calls a "smashing culture" - a blunt but effective way of solving problems. He has found hundreds of snails and hard-shelled fruits smashed for food, seen chimps carrying termite mounds to rocks to break them open and also found a turtle that was almost certainly smashed apart by chimps.

    Like chimp populations in other parts of Africa, the Bili chimps use sticks to fish for ants, but here the tools are up to 2.5 metres long.

    All these observations of chimpanzee behavioral diversity are pretty exciting, since they really provide an interesting model of early hominid diversification. Longstanding subspecies-level populations with strong behavioral differences involving food collection and diet may describe both A. afarensis (along with regional variants) and Late Pliocene Homo.

    A mention is in the article about whether they should be considered a new (fifth) chimpanzee subspecies. I'd say that's probably a given at this point; doubtless the Fongoli chimpanzees will become a sixth.

    Do they deserve it? Well, I suppose they're at least as distinct as the others behaviorally and anatomically, which isn't saying much. Genetically, it's an open question so far, but I wouldn't be surprised if they were as distinct as central and eastern chimpanzees, and certainly moreso than P. t. vellerosus. It's hard for me to see where ape subspecies taxonomy is going to end, since there are few scientific interests vested against further taxonomizing. Sure, there are conservatives, but none with enough firepower to roll back P. t. vellerosus, apparently. So, more subspecies lie in our future: I would guess two or three more for Bornean orangutan populations and who knows how many Western lowland gorilla populations will qualify?

    (via Gene Expression)

    Tags: 
    chimpanzees
    Pliocene
    A. afarensis

  • HIV susceptibility locus protects against an extinct virus

    Sun, 2007-06-24 20:07 -- John Hawks

    What's behind the headline about "resurrecting an ancient virus"?

    The study, which appears tomorrow in Science, focuses on Pan troglodytes endogenous retrovirus (PtERV1). More than 100 copies of inactive PtERV1 are sprinkled throughout the chimpanzee and gorilla genomes, whereas humans have none. "About 4 million years ago, this virus was active and independently infecting all these species, but not humans," says virologist Michael Emerman, who conducted the study with evolutionary biologist Harmit Malik and postgraduate student Shari Kaiser, all of whom work at the Fred Hutchinson Cancer Research Center in Seattle, Washington.

    That's a pretty radical genome-wide difference between humans and the African apes. It's interesting that the chimpanzee and gorilla lineages were capable of exchanging viruses from early in their evolution. If they are right about the 4 Ma age, that is about halfway between the common ancestor of chimpanzees and gorillas (around 7--10 Ma) and today. Since they still exchange viruses today (including Ebola), you might think that it wouldn't be surprising that they did so in the Pliocene. But I think it's important because it establishes sympatry of the two apes: the ancestors of today's chimpanzees and gorillas lived in the same geographic region. If the two lineages originated in an allopatric speciation, then they had expanded their ranges by the Pliocene to overlap with each other. And sympatry means that they must have been adaptively differentiated by that time.

    The now-extinct virus was interesting to this research group for another reason: apparently, a protein essential to HIV resistance in other primates lets humans down by being resistant to the extinct virus. This is a pretty tricky storyline, so I'll try to explain. The protein is named TRIM5α, it is key to the immune response to viruses. The human form of the protein does not do a good job of fighting HIV, and some other primates have a form that resists HIV infection must more effectively. So this protein has been a focus of HIV research.

    When Kaiser and colleagues examined the sequences of the ancient retrovirus imprisoned in the chimpanzee genome, they found that one of the virus' genes interacts with TRIM5α. Prior work had established the variation among primates in TRIM5α's response to HIV. Now, they found that no known primate TRIM5α sequence provides an effective response to both HIV and the ancient chimpanzee virus.

    In other words, this ancient chimpanzee virus, PtERV1, is like the immune system equivalent of Bizarro Superman -- it's just the opposite of the real thing.

    In terms of hominid evolution, there is the obvious question of why humans never acquired the many endogenous copies of this viral genome. Clearly, ancient hominids did not have the virus in substantial enough numbers to result in its incorporation into our genome. But why not? In particular, did our TRIM5α sequence protect us?

    Here's what Kaiser and colleagues have to say:

    Although we cannot rule out the possibility that PtERV1 never infected human ancestors for other reasons (SOM Text, note 1), our data do suggest the possibility that TRIM5 was fixed in human populations because of its ability to confer protection against PtERV1 (Figs. 2 and 3) and that modern humans have descended from ancestors who resisted infection. Indeed, we know that there is very little diversity in the human population today in the part of TRIM5 that determines antiviral specificity (6, 16, 17). However, we find that chimpanzee TRIM5 is also capable of restricting PtERV1 and encodes an R332 (Fig. 3), yet chimpanzees contain multiple copies of PtERV1 in their genome and humans do not. Moreover, we find that R332 is monomorphic in the TRIM5 allele in all four subspecies of chimpanzees and in bonobos, which indicates that R332 is evolutionarily conserved through the chimpanzee radiation (in the past 1 to 2 million years). The most parsimonious explanation for the presence of R332 in humans and chimpanzees is that the mutation was fixed in our common ancestor, which presents a paradox because chimpanzee TRIM5 did not protect them against PtERV1. This suggests that TRIM5 alone does not determine retroviral invasion into the germline but that the combination of multiple retroviral restriction factors that are also rapidly evolving, such as the Apobec3 family (18), are necessary to explain ancient transmission events.

    Well, no one can say for sure, but I think it seems pretty unlikely that the hominid TRIM5α gene is the result of selection against infection by this particular virus. The chimpanzee and gorilla genomes have more than 100 copies of the viral DNA in their genomes, which means that it was a long-term infectious agent in those lineages, and its genome was often incorporated into its hosts' germlines. It is probable that these viral genes evolved neutrally after being incorporated into the chimpanzee and gorilla genomes: if they were deleterious, they would be gone; if they were adaptive, they would probably be more highly conserved. Neither chimpanzees nor gorillas are known to carry the live virus today, which is therefore presumed to be extinct. If true, that means that both chimpanzees and gorillas lost the virus, probably sometime before 3 million years ago. This loss occurred either because of convergent genetic adaptations in both lineages (I say convergent because they may or may not have involved the same genes), or because of extreme bottlenecks during which the longtime viral parasites were lost by chance.

    Now, consider some hypotheses:

    Hypothesis 1: The virus was a longtime hominid pathogen, to which TRIM5α was an adaptation. If this were true, then the human genome ought to harbor at least some copies of the viral DNA. It has none. So this hypothesis probably isn't true.

    Hypothesis 2: The virus was a severe short-term epidemic in ancient hominids, and we are descended from the only survivors, who happened to have a resistant TRIM5α allele. This is the hypothesis proposed in the quote above. If this were true, then we wouldn't necessarily expect to see copies of the viral genome in human DNA -- the infection and population crash may have happened too fast. But a single epidemic, or even a succession of several epidemics of the virus, would be unlikely to fix a variant allele. After all, neither the Black Death nor smallpox, nor any other historical epidemic has managed such a feat. And viruses with such exceptionally high death tolls do not tend to sustain epidemics through sparse populations like ancient hominids. Indeed, it seems likely that the virus' long survival in chimpanzees and gorillas implies that its hosts survived for a long time with the virus, and dispersed it as they encountered other individuals over time. If the virus let its hominid victims live a long time and thereby spread across low-density hominid populations, then there ought to be at least some copies of it in our genomes. And there aren't any. Also, the TRIM5α protein has a strong signature of positive selection in the human lineage, which means that there have been multiple selected substitutions. Multiple substitutions are very unlikely to have happened simultaneously; it is more likely that they occurred sequentially, taking a long time. So this hypothesis probably isn't true, either.

    Hypothesis 3: The virus never infected hominids, who were, after all, allopatric from chimpanzees and gorillas. Instead, some other virus -- or more probably, several viruses -- infecting ancient hominids explain the evolution of the human TRIM5α gene.

    I like hypothesis 3 the best; the data don't seem to reject it. Humans are not very susceptible to the PtERV1 virus. Indeed, our own TRIM5α variant, alone or with other genetic adaptations, have have helped to prevent the virus from infecting ancient hominids at all. Or maybe our ancestors never encountered the virus and our TRIM5α is a result of later events.

    I should add, from a quick look at Sawyer et al. 2005, that chimpanzees and gorillas share at least one parallel amino acid subsitution in the rapidly-evolving SPRY domain of TRIM5α -- at position 340. The current paper (Kaiser et al. 2007) notes that humans and chimpanzees share a derived amino acid substitution at position 332. That position (332) is important because the biochemical work by Kaiser et al. 2007 and others has shown it is a critical site for human susceptibility to HIV:

    For example, the amino acid at position 332 within this patch is a critical determinant of HIV-1 restriction (13). Humans and chimpanzees encode an arginine (R) residue at position 332, whereas the hominoid ancestral residue at this position is a glutamine (Q). Reversing this change (R332Q) had moderate effects on the ability of human TRIM5α to restrict MLV variants (fig. S2). Notably, changing the arginine to the ancestral glutamine abolished the ability of human TRIM5α to efficiently restrict PtERV1 infectivity (Fig. 2B). Unexpectedly, the R332Q mutation had the opposite effect on HIV-1, improving the ability of human TRIM5α to restrict this virus (15) (Fig. 2B). Thus, the R332Q mutation in human TRIM5α reveals a trade-off in TRIM5α's ability to restrict two retroviruses; a mutation that abolished restriction for PtERV1 results in a gain of restriction to other viruses such as HIV-1.

    It would be interesting to see what difference the chimpanzee and gorilla alleles at position 340 make; perhaps their TRIM5α protein remains constrained by selection from yet another pathogen?

    In any case, during the last few years we have learned a great deal about ancient selection in hominids associated with pathogens. And most of what has come out has been gross changes such as pseudogenization. In this instance, the key information comes from a genomic comparison showing the huge importance of an ancient pathogen in both chimpanzees and gorillas, but not humans.

    It is hard to overstate just how glaring these comparisons are -- they are not at all subtle. If most genetic changes during human evolution have been like precision-aimed shots from a sniper rifle, these disease-associated adaptations we've been finding are like blasts from a cannon.

    So there is a lot left to discover.

    UPDATE (2009/06/19): The original finding that PTERV1 dates to an ancient retroviral infection in chimpanzees and gorillas was found by Yohn et al. (2005). From the abstract:

    Phylogenetic analysis of the endogenous retrovirus reveals that the gorilla and chimpanzee elements share a monophyletic origin with a subset of the Old World monkey retroviral elements, but that the average sequence divergence exceeds neutral expectation for a strictly nuclear inherited DNA molecule. Within the chimpanzee, there is a significant integration bias against genes, with only 14 of these insertions mapping within intronic regions. Six out of ten of these genes, for which there are expression data, show significant differences in transcript expression between human and chimpanzee. Our data are consistent with a retroviral infection that bombarded the genomes of chimpanzees and gorillas independently and concurrently, 3–4 million years ago. We speculate on the potential impact of such recent events on the evolution of humans and great apes.

    This paper includes much speculation about the role of retroviruses in promoting bursts of adaptation in ancient chimpanzees and gorillas. That has been a topic of further research, as well.

    References:

    Kaiser SI, Malik HS, Emerman M. 2007. Restriction of an extinct retrovirus by the human TRIM5α antiviral protein. Science 316:1756-1758. doi:10.1126/science.1140579

    Sawyer SL, Wu LI, Emerman M, Malik HS. 2005. Positive selection of primate TRIM5α identifies a critical species-specific retroviral restriction domain. Proc Nat Acad Sci USA 102:2832-2837. doi:10.1073/pnas.0409853102

    Yohn CT, Jiang Z, McGrath SD, Hayden KE, Khaitovich P, et al. 2005. Lineage-Specific Expansions of Retroviral Insertions within the Genomes of African Great Apes but Not Humans and Orangutans. PLoS Biol 3(4): e110. doi:10.1371/journal.pbio.0030110

    Tags: 
    ancient DNA
    chimpanzees
    Pliocene

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