Human evolutionary ecological theory and research pertaining to antagonists (parasites and predators) is less extensively developed than that pertaining to resources such as food. Moreover, evolutionary socioecology linking parasites in particular to specific kinds of social organization is even less so. On these two grounds alone the target article by Fincher & Thornhill (F&T), reviewing the theory and evidence that high parasite-stress is associated with positively assortative sociality in humans and extending it to include strong family ties and heightened religiosity, is welcome. I will not comment one way or another on that specific theory or the evidence for it but confine my comments instead to the more general theory placed between these two aspects, because it is less precise than is required in one respect, and perhaps more circuitous than is required in another.
The more general theory attributes an association between parasite stress and assortative sociality to ancestrally adaptive genetic evolution of condition-dependent phenotypic plasticity, including, but not restricted to, the case in which culture mediates the selection pressure from parasites. On the first point, condition-dependent adaptive phenotypic plasticity is attributed to local variation, change, and complexity. However, variation and change on a scale between individuals/generations would simply result in the direction of selection varying and changing. It is environmental uncertainty, and on a scale within individuals/generations, that is necessary for adaptive plasticity. Even that is not sufficient for condition-dependent adaptive plasticity, because simple environmental uncertainty favors plasticity of the probability-matching type in which behaviors are emitted at random, but with a probability matching that of the environmental conditions to which they are adapted. Specifically, condition-dependent adaptive phenotypic plasticity requires (i) environmental uncertainty; (ii) such uncertainty on the correct small scale; and (iii) that the uncertainty nevertheless be accompanied by reliable cues (Roff Reference Roff2002, Ch. 6).
On the possible role of culture, that people choose their values is far from the “traditional sociological view,” or the anthropological one for that matter (and note that the Jost et al. [Reference Jost, Federico and Napier2009] review cited by F&T [sect. 2.1, para. 11] is from the psychological literature on the social psychology of political ideology). F&T share a common misconception that the books by Cavalli-Sforza and Feldman (Reference Cavalli-Sforza and Feldman1981), Lumsden and Wilson (Reference Lumsden and Wilson1981), and Boyd and Richerson (Reference Boyd and Richerson1985) were about coevolution between culture and genes. The Cavalli-Sforza and Feldman book was about purely cultural, not genetic evolution at all. Although referring to coevolution, the Lumsden and Wilson book was about how genes create rules which bias the cultural alternatives preferred by individuals (along the lines favored in this article minus the emphasis on adaptive plasticity). Boyd and Richerson (Reference Boyd and Richerson1985) called their theory a dual inheritance, not a dual evolutionary one. Although they included sociocultural selection under the label of “biased transmission” (direct, indirect, and positively frequency-dependent), biological and sociocultural adaptedness were commonly implicitly equated and the authors were very concerned with the biological evolution of human capacities for individual learning, cultural transmission, and cultural selection. In none of these books were genes and culture really understood as both varying, being transmitted, being selected and hence evolving, and to be doing so in interaction with each other (for reviews and summaries of the originals, see Blute Reference Blute1987). The first extensive treatment of coevolution in this full sense was Durham (Reference Durham1991) who, in the context of a series of anthropological case studies, described genes selecting among cultural alternatives as “genetic mediation” and cultural alternatives selecting among genes as “cultural mediation” – both of which were once, and mostly still are, called gene-culture coevolution, but what some today, including the authors of the present target article, distinguish as gene-culture and culture-gene coevolution, respectively. To bring the latter up to date, Laland et al. (Reference Laland, Odling-Smee and Myles2010) recently reviewed more than a hundred human genes organized into eight functional groups whose evolution can plausibly be attributed to cultural selection pressures.
The version of culture-gene coevolution presented in F&T's article is one in which parasites select for human cultural practices, which in turn select for human genes affecting psychological states, which in turn promote those cultural practices. The insertion of human genetic differences in the middle in this way is logically wholly unnecessary to a possible coevolutionary interpretation. Because culture is not only transmitted but can also vary, be selected, and therefore literally evolve (e.g., Blute Reference Blute2010), and because the bulk of the cultural practices involved are transmitted roughly vertically, making them generally biologically adaptive (Blute Reference Blute2006), alternative genes in parasites can select for alternative biologically adaptive anti-parasitic cultural practices in humans directly. Human genetic differences might conceivably mediate this process in some cases. That depends on whether or not there is (or was) additive genetic variance in humans for most of the psychological states/behavioral traits in question. Given that most of the heritability of complex diseases even is “missing” in genome-wide association studies (Manolio et al. Reference Manolio, Collins, Cox, Goldstein, Hindorff, Hunter, McCarthy, Ramos, Cardon, Chakravarti, Cho, Guttmacher, Kong, Kruglyak, Mardis, Rotimi, Slatkin, Valle, Whittemore, Boehnke, Clark, Eichler, Gibson, Haines, Mackay, McCarroll and Visscher2009), most social scientists remain skeptical. But the truth is that for the vast majority of cases, nobody really knows either way.
On the simpler direct coevolutionary interpretation, a parasite stress theory of assortative sociality would still remain a particularly interesting case. That is because, on the one hand, like the original biological concept of purely genetic coevolution between species, it would be interspecific. On the other hand, like the original concept of gene-culture coevolution in humans, it would be between genes and culture. So it would be unique in either coevolution literatures, because it would be one of interspecific gene-culture coevolution – that is, of genes in one or more species evolving in interaction with cultural elements in another. On these grounds, too, I very much appreciate the authors having presented this theory.
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Human evolutionary ecological theory and research pertaining to antagonists (parasites and predators) is less extensively developed than that pertaining to resources such as food. Moreover, evolutionary socioecology linking parasites in particular to specific kinds of social organization is even less so. On these two grounds alone the target article by Fincher & Thornhill (F&T), reviewing the theory and evidence that high parasite-stress is associated with positively assortative sociality in humans and extending it to include strong family ties and heightened religiosity, is welcome. I will not comment one way or another on that specific theory or the evidence for it but confine my comments instead to the more general theory placed between these two aspects, because it is less precise than is required in one respect, and perhaps more circuitous than is required in another.
The more general theory attributes an association between parasite stress and assortative sociality to ancestrally adaptive genetic evolution of condition-dependent phenotypic plasticity, including, but not restricted to, the case in which culture mediates the selection pressure from parasites. On the first point, condition-dependent adaptive phenotypic plasticity is attributed to local variation, change, and complexity. However, variation and change on a scale between individuals/generations would simply result in the direction of selection varying and changing. It is environmental uncertainty, and on a scale within individuals/generations, that is necessary for adaptive plasticity. Even that is not sufficient for condition-dependent adaptive plasticity, because simple environmental uncertainty favors plasticity of the probability-matching type in which behaviors are emitted at random, but with a probability matching that of the environmental conditions to which they are adapted. Specifically, condition-dependent adaptive phenotypic plasticity requires (i) environmental uncertainty; (ii) such uncertainty on the correct small scale; and (iii) that the uncertainty nevertheless be accompanied by reliable cues (Roff Reference Roff2002, Ch. 6).
On the possible role of culture, that people choose their values is far from the “traditional sociological view,” or the anthropological one for that matter (and note that the Jost et al. [Reference Jost, Federico and Napier2009] review cited by F&T [sect. 2.1, para. 11] is from the psychological literature on the social psychology of political ideology). F&T share a common misconception that the books by Cavalli-Sforza and Feldman (Reference Cavalli-Sforza and Feldman1981), Lumsden and Wilson (Reference Lumsden and Wilson1981), and Boyd and Richerson (Reference Boyd and Richerson1985) were about coevolution between culture and genes. The Cavalli-Sforza and Feldman book was about purely cultural, not genetic evolution at all. Although referring to coevolution, the Lumsden and Wilson book was about how genes create rules which bias the cultural alternatives preferred by individuals (along the lines favored in this article minus the emphasis on adaptive plasticity). Boyd and Richerson (Reference Boyd and Richerson1985) called their theory a dual inheritance, not a dual evolutionary one. Although they included sociocultural selection under the label of “biased transmission” (direct, indirect, and positively frequency-dependent), biological and sociocultural adaptedness were commonly implicitly equated and the authors were very concerned with the biological evolution of human capacities for individual learning, cultural transmission, and cultural selection. In none of these books were genes and culture really understood as both varying, being transmitted, being selected and hence evolving, and to be doing so in interaction with each other (for reviews and summaries of the originals, see Blute Reference Blute1987). The first extensive treatment of coevolution in this full sense was Durham (Reference Durham1991) who, in the context of a series of anthropological case studies, described genes selecting among cultural alternatives as “genetic mediation” and cultural alternatives selecting among genes as “cultural mediation” – both of which were once, and mostly still are, called gene-culture coevolution, but what some today, including the authors of the present target article, distinguish as gene-culture and culture-gene coevolution, respectively. To bring the latter up to date, Laland et al. (Reference Laland, Odling-Smee and Myles2010) recently reviewed more than a hundred human genes organized into eight functional groups whose evolution can plausibly be attributed to cultural selection pressures.
The version of culture-gene coevolution presented in F&T's article is one in which parasites select for human cultural practices, which in turn select for human genes affecting psychological states, which in turn promote those cultural practices. The insertion of human genetic differences in the middle in this way is logically wholly unnecessary to a possible coevolutionary interpretation. Because culture is not only transmitted but can also vary, be selected, and therefore literally evolve (e.g., Blute Reference Blute2010), and because the bulk of the cultural practices involved are transmitted roughly vertically, making them generally biologically adaptive (Blute Reference Blute2006), alternative genes in parasites can select for alternative biologically adaptive anti-parasitic cultural practices in humans directly. Human genetic differences might conceivably mediate this process in some cases. That depends on whether or not there is (or was) additive genetic variance in humans for most of the psychological states/behavioral traits in question. Given that most of the heritability of complex diseases even is “missing” in genome-wide association studies (Manolio et al. Reference Manolio, Collins, Cox, Goldstein, Hindorff, Hunter, McCarthy, Ramos, Cardon, Chakravarti, Cho, Guttmacher, Kong, Kruglyak, Mardis, Rotimi, Slatkin, Valle, Whittemore, Boehnke, Clark, Eichler, Gibson, Haines, Mackay, McCarroll and Visscher2009), most social scientists remain skeptical. But the truth is that for the vast majority of cases, nobody really knows either way.
On the simpler direct coevolutionary interpretation, a parasite stress theory of assortative sociality would still remain a particularly interesting case. That is because, on the one hand, like the original biological concept of purely genetic coevolution between species, it would be interspecific. On the other hand, like the original concept of gene-culture coevolution in humans, it would be between genes and culture. So it would be unique in either coevolution literatures, because it would be one of interspecific gene-culture coevolution – that is, of genes in one or more species evolving in interaction with cultural elements in another. On these grounds, too, I very much appreciate the authors having presented this theory.