Gorillas and ebola

Just a pointer to this Reuters article about the spread of the Ebola virus through a wild gorilla population:

A 2004 outbreak of the virus, which also kills people, killed 97 percent of gorillas who lived in groups and 77 percent of solitary males, Damien Caillaud and colleagues from the University of Montpellier and the University of Rennes in France reported.
Overall, it wiped out 95 percent of the gorilla population within a year, they reported in the journal Current Biology.

The paper in Current Biology (DOI link) is super-short, and ends with this paragraph:

These results provide new insights into the epidemiology of a still largely unknown disease. In an evolutionary perspective, this study provides direct evidence that, in hominoids other than humans, group individuals face a higher disease risk. This cost has probably been an important constraint to sociality evolution in early humans [10]. In a conservation perspective, the demographic impact of Ebola virus is dramatically enhanced since it disproportionately affects females and young individuals, which are essential for population recovery (Figure 2C,D). Censuses conducted in 19945 revealed that Odzala-Kokoua National Park gorilla density was the highest ever recorded, averaging 5.4 ind/km2 [11]. Preliminary surveys we conducted show that EBOV may have affected this population heterogeneously, with some large areas being now almost devoid of gorillas and others seeming intact. Thousands of gorillas have probably disappeared. As the impact of EBOV on apes is still difficult to control, reinforced protection of gorillas and chimpanzees is required throughout their range, especially against poaching and logging, the two major additional threats to these species [6] (Caillaud et al. 2006:R490, emphases mine).

This kind of risk from living in a social group would probably strike most people as highly irregular. I mean, how often can a killer virus come through? Maybe it is a unique recent risk because of human activities that incur on gorilla habitat.

On the other hand, a disease doesn't have to be so deadly to have important impacts on fitness, and sociality also has the increased risk of parasites (reviewed by Altizer et al. 2003). This passage from Semple and colleagues (2002) applies to primates:

However, many studies have identified social and ecological correlates of parasite abundance and disease prevalence that would be predicted to play a role in shaping the evolution of the immune system.
Two parameters of particular interest in this respect are population density and group size, which may affect parasite transmission rate between hosts. Comparative analysis has indicated that parasite abundance can be strongly correlated with host population density among mammals (Arneberg et al. 1998), and meta-analysis has demonstrated that the prevalence and intensity of contagious parasites can be positively correlated with host group size
among social animals (Cote & Poulin 1995). More specifically among primates, prevalence of parasitic infection has been found to increase with higher population density (e.g. howler monkeys; Stuart et al. 1990), and group size has been found to be positively related to parasitic infection rate (e.g. Amazonian primates; Davies et al. 1991).

Epidemics may be a more serious risk for primates than for many other mammals; since:

  1. primates are highly social
  2. multiple primate species are often sympatric (chimpanzees and gorillas being the operant example here, although both are widely sympatric with cercopithecine and colobine species also)
  3. primates interact more closely than most other mammals with bats and birds, the major long-distance disease dispersers

This is one of the problems with optimality models for group dynamics -- you never know which important variables you are leaving out.

For instance, why don't orangutan social groups spend much time around each other? The usual answer is that it is energetically expensive to forage together through much of their habitat. But then, there is this:

Sylvatic transmission of arboviruses among Bornean orangutans
ND Wolfe, AM Kilbourn, WB Karesh, HA Rahman, EJ Bosi, BC Cropp, M Andau, A Spielman, and DJ Gubler
Wild populations of nonhuman primates live in regions of sylvatic arbovirus transmission. To assess the status of arbovirus transmission in Bornean forests and the susceptibility of wild orangutans to arboviral infection, blood samples of wild orangutans, semi-captive orangutans, and humans were examined. Samples were tested by plaque reduction neutralization test for antibodies to viruses representing three families (Flaviviridae, Alphaviridae, and Bunyaviridae), including dengue-2, Japanese encephalitis, Zika, Langat, Tembusu, Sindbis, Chikungunya, and Batai viruses. Both wild and semi-captive orangutan groups as well as local human populations showed serologic evidence of arbovirus infection. The presence of neutralizing antibodies among wild orangutans strongly suggests the existence of sylvatic cycles for dengue, Japanese encephalitis, and sindbis viruses in North Borneo. The present study demonstrates that orangutans are susceptible to arboviral infections in the wild, although the impact of arboviral infections on this endangered ape remain unknown.

A habit for avoiding social contacts might be expected to reduce the risk of infection, just as it did for gorillas faced with Ebola. This strategy may well be resource-mediated: relatively low local resource densities may restrict any advantages of high social contacts to an extent that the benefits for resisting disease outweigh them. In other words, disease is not the only factor encouraging low social contacts, but it may modify the balance among the other factors in ecology-dependent ways.

The strategy may also be body mass-mediated. For instance, Davies et al. (1991) found that malaria risk in New World primates depends not only on group size but also body weight. Semple et al. 2002 also show that body size and immune system activity are also related to disease and infection rates.

On the other hand, Bonds and colleagues (2005) describe a model in which higher disease prevalence can increase the advantages of sociality. There is some entertaining dancing at the end of that paper, since empirical studies have pretty consistently shown a positive association between disease risk and social group size -- but Bonds et al. argue that these studies aren't finding evolutionary responses, but instead positive relationships that are expected within static populations. Whatever the case, there is some interesting math in this paper, which has the chief weakness of assuming that the host population is homogeneous. Working out optima with different host strategies possible would be more difficult but worthwhile -- for instance, a long solitary period for males would be a strategy that appears to be adaptive in the gorilla-Ebola case, and plausibly is generally so for large-bodied primates.

At any rate, this area of research is developing quickly. In 2002, Kappeler and van Schaik reviewed determinants of sociality in primates and had only this to say about disease:

Finally, potential main determinants of some aspects of social systems, as well as some important consequences, remain virtually unexplored. There are few studies on diseases of natural primate populations, and their effects on behavior (Freeland, 1976; Davies et al., 1991; Heymann, 1999; Nunn et al., 2000) (Kappeler and van Schaik 1998:728).

There have been several studies in the interim, including some of the ones listed here. A bit more theory, particularly with respect to variability in strategies and multispecific interactions, would help. And of course, there is the possibility that direct adaptations to diseases had important effects on social group sizes. This is where I think there may be important impacts on human evolution, since we seem to have had some fairly unique immune system adaptations during the course of the last couple million years.

References:

Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC. 2003. Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Systematics 34:517-547. DOI link

Bonds MH, Keenan DC, Leidner AJ, Rohani P. 2005. Higher disease prevalence can induce greater sociality: a game theoretic coevolutionary model. Evolution 59:1859-1866. Abstract

Caillaud D and 8 others. 2006. Gorilla susceptibility to Ebola virus: the cost of sociality. Curr Biol 16:R489-R491. DOI link

Davies CR, Ayres JM, Dye C, Deane LM. 1991. Malaria infection rate of Amazonian primates increases with body weight and group size. Functional Ecology 5:655-662.

Kappeler PM, van Schaik CP. 2002. Evolution of primate social systems. Int J Primatol 23:707-740. DOI link

Semple S, Cowlishaw G, Bennett PM. 2002. Immune system evolution among anthropoid primates: parasites, injuries and predators. Proc Roy Soc B 269:1031-1037. DOI link

Wolfe ND and 8 others. 2001. Sylvatic transmission of arboviruses among Bornean orangutans. Am J Trop Med Hyg 64:310-316. Abstract