How evolutionary behavioural sciences can help us understand behaviour in a pandemic.

The COVID-19 pandemic has brought science into the public eye and to the attention of governments more than ever before. Much of this attention is on work in epidemiology, virology and public health, with most behavioural advice in public health focusing squarely on 'proximate' determinants of behaviour. While epidemiological models are powerful tools to predict the spread of disease when human behaviour is stable, most do not incorporate behavioural change. The evolutionary basis of our preferences and the cultural evolutionary dynamics of our beliefs drive behavioural change, so understanding these evolutionary processes can help inform individual and government decision-making in the face of a pandemic. Lay summary: The COVID-19 pandemic has brought behavioural sciences into the public eye: Without vaccinations, stopping the spread of the virus must rely on behaviour change by limiting contact between people. On the face of it, "stop seeing people" sounds simple. In practice, this is hard. Here we outline how an evolutionary perspective on behaviour change can provide additional insights. Evolutionary theory postulates that our psychology and behaviour did not evolve to maximize our health or that of others. Instead, individuals are expected to act to maximise their inclusive fitness (i.e, spreading our genes) - which can lead to a conflict between behaviours that are in the best interests for the individual, and behaviours that stop the spread of the virus. By examining the ultimate explanations of behaviour related to pandemic-management (such as behavioural compliance and social distancing), we conclude that "good of the group" arguments and "one size fits all" policies are unlikely to encourage behaviour change over the long-term. Sustained behaviour change to keep pandemics at bay is much more likely to emerge from environmental change, so governments and policy makers may need to facilitate significant social change - such as improving life experiences for disadvantaged groups.

Evolution of the bitter taste receptor TAS2R38 in colobines.

Bitter taste perception enables the detection of potentially toxic molecules and thus evokes avoidance behavior in vertebrates. It is mediated by bitter taste receptors, TAS2Rs. One of the best-studied TAS2R is TAS2R38. Phenylthiocarbamide (PTC) perception and TAS2R38 receptors vary across primate species, and this variation may be related to variation in dietary preferences. In particular, we previously found that the low sensitivity of TAS2R38s in Asian colobines likely evolved as an adaptation to their leaf-eating behavior. However, it remains unclear whether this low PTC sensitivity is a general characteristic of the subfamily Colobinae, a primate group that feeds predominantly on leaves. We performed genetic analyses, functional assays with mutant proteins, and behavioral analyses to evaluate the general characteristics of TAS2R38 in colobines. We found that PTC sensitivity is lower in TAS2R38s of African colobines than in TAS2R38s of omnivorous macaques. Furthermore, two amino acids shared between Asian and African colobines were responsible for low sensitivity to PTC, suggesting that the last common ancestor of extant colobines had this phenotype. We also detected amino acid differences between TAS2R38s in Asian and African colobines, indicating that they evolved independently after the separation of these groups.

Handedness heritability in industrialized and nonindustrialized societies.

In modern societies, there is a decreased usage of traditional weapons to settle interpersonal or inter-group disputes compared to usage in traditional societies, possibly affecting the frequency-dependent selection on the handedness polymorphism. Another societal difference is the extensive automation of hard manual labour (including agriculture) in industrialized societies, relaxing the selection for hand specialization. Thus, selection of handedness is likely to differ between traditional and modern societies. As heritability determines the relative speed of evolutionary dynamics, handedness heritability was compared between industrialized and non-industrialized societies. First, individuals were sampled from a non-industrialized area in Indonesia, where violent conflicts are relatively frequent and tribal wars have been prevalent recently. Handedness was recorded directly or indirectly for 11,490 individuals belonging to 650 independent pedigrees, and handedness heritability was estimated using a pedigree-based animal model. Second, estimates of handedness heritability derived from published sources were collected to compare heritability estimates, accounting for various confounding variables. Non-industrialized countries displayed a significantly higher heritability value (h2 = 0.56) than that of industrialized countries (h2 = 0.20). Heritability decreased with time along the twentieth century in industrialized countries, independently of the frequency of left-handedness, and independently of the method used to measure handedness. In conclusion, the data are consistent with a decrease in handedness heritability following the industrialization process and/or the associated decrease in violence using traditional weapons. The difference in heritability between industrialized and non-industrialized countries suggests that selection of handedness is thus likely to differ between traditional and modern societies.

Male Homosexual Preference: Femininity and the Older Brother Effect in Indonesia.

Male homosexual preference (MHP) is an evolutionary enigma because it is partially heritable and imposes a fertility cost. In occidental societies, homosexual men are feminized at various levels and they have more older brothers than heterosexual men. To evaluate whether femininity and the fraternal birth order (FBO) effect are universal features of MHP or not, we collected original data from homosexual men, heterosexual men, and heterosexual women from Java (Indonesia). Facial photographs were used to test whether homosexual faces are feminized when compared with heterosexual ones. We found that faces manipulated to resemble the average face of homosexual men are perceived as facially feminized, suggesting that homosexual men are facially feminized compared to heterosexual men, although a higher facial femininity was not captured by morphological analyses. Then, family data were used to detect differences in siblings' composition between homosexuals and heterosexuals. Homosexual men displayed a higher number of older brothers than heterosexual men, even when sibship size was controlled for, suggesting that the FBO effect exists in Indonesian populations. Independent of sexual orientation, men with older brothers seem more feminized than those without older brothers, consistent with the immune origin of the FBO effect. In conclusion, MHP in Indonesia is partially feminized and they have more older brothers. Such features are also associated with MHP in other cultural contexts, suggesting a cross-cultural effect of men homosexual preference. An evolutionary explanation is available for the feminizing effect, although the FBO effect remains unexplained even if proximal mechanisms start to be identified.

Kin Selection and Male Homosexual Preference in Indonesia.

Male homosexual preference (MHP) challenges evolutionary thinking because the preference for male-male relationships is heritable, implies a fertility cost (lower offspring number), and is relatively frequent in some societies (2-6% in Western countries) for a costly trait. It has been proposed that individuals with a MHP counterbalance reproductive costs through the transfer of resources to kin, thereby improving their indirect reproduction through kin's reproductive success. This kin selection hypothesis is not supported in Western countries and Japan, although consistent evidence has been obtained in Samoa. In this study, data from Java (Indonesia) were obtained to assess the avuncular tendencies of men with contrasting sexual orientation to measure possible resource transfer. Consistent with the kin selection hypothesis, males with a homosexual orientation reported an increased willingness to transfer resources toward nephews and nieces and declared having transferred more money to nephews and nieces. We developed a method to quantitatively estimate the contribution of kin selection on inclusive reproduction associated to sexual orientation, taking into account various possible biases. Kin selection reduced the direct reproductive cost of homosexual men by 20%, so suggesting that kin selection alone is insufficient to explain the maintenance of male homosexuality. Other potential factors are discussed, as well as the limitations of the study and the social determinant operating for the expression of increased avuncular tendencies of homosexual men.

Functional characterization of the TAS2R38 bitter taste receptor for phenylthiocarbamide in colobine monkeys.

Bitterness perception in mammals is mostly directed at natural toxins that induce innate avoidance behaviours. Bitter taste is mediated by the G protein-coupled receptor TAS2R, which is located in taste cell membranes. One of the best-studied bitter taste receptors is TAS2R38, which recognizes phenylthiocarbamide (PTC). Here we investigate the sensitivities of TAS2R38 receptors to PTC in four species of leaf-eating monkeys (subfamily Colobinae). Compared with macaque monkeys (subfamily Cercopithecinae), colobines have lower sensitivities to PTC in behavioural and in vitro functional analyses. We identified four non-synonymous mutations in colobine TAS2R38 that are responsible for the decreased sensitivity of the TAS2R38 receptor to PTC observed in colobines compared with macaques. These results suggest that tolerance to bitterness in colobines evolved from an ancestor that was sensitive to bitterness as an adaptation to eating leaves.