Behavioral manipulation: population differences in virulence

Helicobacter pylori (Wikicommons – NIH). Some human populations have become resistant to this bacterium; others have not. Could the same be true for pathogens that manipulate human behavior?



Humans are behavioral creatures par excellence. Our brains oversee a large repertoire of behaviors, each of which is vulnerable to manipulation. We can be manipulated by psychological means, like the parasite who lives off the altruism of others.  There's also ideological manipulation. 

And then there's hardwired manipulation—an organism enters your mind and rewires some of its circuitry. That kind of manipulation is poorly known. We know a lot about short-term infections that make you sick. We know much less about long-term infections where the pathogen hangs around in your body without triggering an immune response. There’s no fever, no rash, no abscess. Yet it may be doing something to the most important organ of your body, perhaps to increase its chances of spreading to another host. Not surprisingly, the adverse effects become worse when you're no longer of much help. It no longer has anything to lose from trashing its host.

So if a pathogen is screwing with your mind, the symptoms will be especially severe in two cases: 

- You’re approaching the end of your life. The pathogen has less incentive to keep you healthy. You’re also less active socially and sexually, and thus less useful as a vehicle for transmission to other hosts.

- The pathogen is spreading out of its original host population and into new hosts that have not had time to develop resistance to its worse effects

This post is about the second case. You pay a cost when a pathogen monkeys around with your mental circuitry. Over time, there will be selection for humans who better resist such manipulation. Eventually, an equilibrium is reached: the pathogen still screws around with your mind, but the negative consequences are kept to a minimum. In most cases. And until it spreads to people who have no resistance.

The latter situation has been covered by a recent review article:

[...] the effects of susceptibility and virulence alleles in the respective gene pools of humans and pathogens are often contingent upon each other. The evolution of virulence is a dynamic process, easily perturbed by extrinsic variables over space and time, and therefore unlikely to follow the same trajectory in every population. [...] Whether the result is a steady-state equilibrium due to a perpetual "arms race" or a commensal detente, the same genes and pathways are unlikely to be involved in every population. As a consequence, when humans and pathogens migrate to new environments or admix, the ensuing disruption of co-evolutionary equilibria and loss of complementarity between host and pathogen genotypes may yield unpredictable and potentially deleterious biomedical consequences. (Kodaman et al. 2014)

The authors cite the example of Helicobacter pylori, a bacterium that lives in the stomach lining. It is a risk factor for gastric cancer, but the level of risk varies according to the population it infects:

Studies of human or H. pylori genetics in isolation have generally failed to explain why populations with similar rates of H. pylori infection exhibit strikingly different susceptibilities to gastric cancer. For example, in many African and South Asian countries, the low incidences of gastric cancer in the presence of almost universal rates of H. pylori infection remain a source of much speculation, and have been referred to collectively as the "African enigma" and the "Asian enigma" [...] In Latin America, where H. pylori strains native to Amerindian populations have been largely displaced by European strains [...], the predominantly Amerindian populations living at high altitudes suffer disproportionately from gastric cancer relative to other populations with similar infection rates [...]. These and other points of evidence raise the possibility that the pathogenicity of a given H. pylori strain may vary with human genomic variation, and that some individuals may be better adapted to their infecting strains than others. (Kodaman et al. 2014)

Manipulating sexual behavior

Pathogens thus differ in their virulence from one human population to another. The same should be true for those pathogens that manipulate human behavior to improve their chances of spreading from one human to another. For them, our most interesting behavior is sex, and the most interesting human populations are "leaky" polygynous ones with high rates of infidelity. In that kind of context they can spread rapidly from one household to another.

Polygyny rates are highest among the tropical farming peoples of sub-Saharan Africa (Dalton and Leung 2011; Pebley and Mbugua 1989). Traditionally, 20 to 40% of all marriages are polygynous, and most women live in polygynous households. Not surprisingly, many men, particularly young men, are single. Their opportunities for sex are limited to rape, affairs with the wives of other men, or abduction of women during times of war:

Typically, the more men are polygynous in a given society, the greater the age difference between husbands and wives. [...] The temporary celibacy of young men in polygynous societies is rarely absolute, however. While it often postpones the establishment of a stable pair-bond and the procreation of children, it often does not preclude dalliance with unmarried girls, adultery with younger wives of older men, or the rape or seduction of women conquered in warfare. Thus, what sometimes looks like temporary celibacy is, in fact, temporary promiscuity. (van den Berghe 1979, pp. 50-51)

Cuckold envy: a case of behavioral manipulation?

This is the environment in which a sexually transmitted pathogen can leapfrog from one polygynous household to another. The main obstacle is male jealousy and male "guarding behavior." The pathogen can increase its chances of transmission by disabling mate guarding or, better yet, reversing it. This kind of host manipulation has been shown in a non-human species: male isopods no longer guard their mates when they get infected by a certain parasite (Mormann, 2010).

In a human context, a pathogen may reverse male jealousy and make its host want to be cuckolded, as a means to gain access to more hosts (Frost 2013). Many sexual fetishes are mentioned in ancient writings: pedophilia, cunnilingus, fellatio, and bestiality, but not cuckold envy. The oldest mentions go back to seventeenth-century England (Kuchar, 2011, pp. 18-19).

Perhaps a sexually transmitted pathogen came to England from West Africa during the early days of the slave trade. Such a pathogen would have evolved in a context where most women were in polygynous marriages and where cuckoldry was the main route for invading one set of wives after another. Meanwhile, the human hosts may have evolved some kind of resistance, perhaps through “overwiring.” Or perhaps a certain level of cuckoldry became socially accepted. No such resistance, however, had evolved in England or elsewhere in the Western world.

As time goes on, we will discover that many STDs have evolved a capacity for behavioral manipulation, specifically by making the host either more promiscuous or less jealous.


References

Dalton, J.T., and T.C. Leung. (2011). Why is Polygyny More Prevalent in Western Africa?
An African Slave Trade Perspective,
http://www.wfu.edu/~daltonjt/PolygynySlaveTrade.pdf

Frost, P. (2013). First, sexual transmissibility and then …? Evo and Proud, January 5
http://evoandproud.blogspot.com/2013/01/first-sexual-transmissibility-and-then.html 

Kodaman, N., R.S. Sobota, R. Mera, B.G. Schneider, and S.M. Williams. (2014). Disrupted human-pathogen co-evolution: a model for disease. Frontiers in Genetics 25 August
https://www.frontiersin.org/articles/10.3389/fgene.2014.00290/full

Kuchar, G. (2001). Rhetoric, Anxiety, and the Pleasures of Cuckoldry in the Drama of Ben Jonson and Thomas Middleton. Journal of Narrative Theory 31(1): 1-30.

Mormann, K. (2010). Factors influencing parasite-related suppression of mating behavior in the isopod Caecidotea intermedius, Theses and Dissertations, paper 48
http://via.library.depaul.edu/etd/48  

Pebley, A. R., and W. Mbugua. (1989). Polygyny and Fertility in Sub-Saharan Africa. In R. J. Lesthaeghe (ed.), Reproduction and Social Organization in Sub-Saharan Africa, Berkeley: University of California Press, pp. 338-364.

van den Berghe, P.L. (1979). Human Family Systems. An Evolutionary View. New York: Elsevier.