Culture changes selection on functional genes

Among the processes of gene–culture coevolution, attention has overwhelmingly focussed on relationships between the distributions of functional genes within a population and cultural variants. Correlations are expected if cultural innovations alter the selection regimes for particular genes, as individuals with the same genes can have different fitness in different cultural contexts. Given it is impossible to demonstrate the causes of past episodes of adaptive evolution experimentally, the strongest evidence comes from humans, where extensive genetic sampling can be combined with historical and archaeological data. For example, the coevolutionary relationship between dairy farming and adult lactase production is well-established47. More generally, diverse agricultural practices are thought to have inadvertently selected for alleles expressed in enhanced metabolism of the increased starch, carbohydrates, alcohol and so forth, found in agricultural diets31,48. Genomic studies have identified over 100 other variants subject to recent selection for which cultural practices are thought to be the primary source of selection, although the difficulty of demonstrating their causal role precludes certainty48.

In non-humans, the most-compelling evidence comes from killer whales, in which recent population-genomic studies show that functional genes associated with digestion differ between ecotypes (Box 1) in ways that appear adaptive, and show evidence of recent selection42,43. Genes associated with the methionine cycle, which is involved in protein synthesis, differ systematically between mammal-eating and fish-eating ecotypes, a contrast presumed to result from different patterns of dietary protein intake42. Although North Pacific and Antarctic mammal-eating ecotypes both had strong signatures of selection in these groups of genes, the precise locations of the variations were different in the two ecotypes, suggesting independent genetic routes to phenotypic change. Given the culturally mediated variation in inter-population variation in chimpanzee (Pan troglodytes) diets49, similar culturally initiated genetic variation in digestion may well be found in this species too.

Culturally transmitted foraging preferences might also have influenced the evolution of functional genes in great tits15,50. Providing food for these birds is popular in the United Kingdom and recent genomic comparisons of British great tits with those from the Netherlands, where bird feeding is less common, suggest there has been selection on genes involved in beak morphology50. Birds that use feeding stations have larger beaks, perhaps because these individuals are more effective at breaking open the provided seeds. Parid tits became famous for their foraging innovations when they learned to pierce open milk bottles to drink the cream in 1940’s Britain; this behaviour spread too rapidly to be the result of individual learning alone51. Artificial seeding of foraging behaviours in great tits has subsequently demonstrated that detecting and learning how to access bird feeders can spread horizontally and vertically through populations via social learning, enhancing individual learning15. It is therefore probable that social transmission of information about seed feeders increased their use quickly, and consequently altered selection pressure for beak size in great tits50. Furthermore, genetic differences within and between populations could affect culture reciprocally; through their positions in social foraging networks50,52, larger-beaked individuals may be more likely to spread knowledge of new feeding opportunities53.

Although genomic scans suggest large-scale culturally driven selection for genes in recent human evolution, with a few exceptions, such as the dairy farming-lactase case, further work is required to pin down particular instances46,54. This is also the case with non-humans where, for instance, it is necessary to exclude the theoretical possibility that ‘allele-surfing’ (i.e., increases in allele frequencies during post-bottleneck population growth) could have contributed to the patterns found in killer whales55.

Culture favours genes enhancing adaptations for culture

A substantial reliance on social learning has been predicted to select for genetic variants that enhance such learning species-wide, shaping supportive neural traits such as encephalisation, energy production or plasticity, or modifying life-history traits such as a longer juvenile period available for learning or enhanced parental support. 'Cultural drive’ or ‘cultural intelligence’ hypotheses2,37,56,57,58,59,60,61,62 cite a range of evidence that cultural inheritance can enhance fitness through the development of greater competence in key behaviours such as foraging and predator avoidance56,59, and they propose that this in turn will enhance selection pressures for genetically coupled phenotypic traits particularly the neural and life-history variables mentioned above. These effects may in turn lead to more reliance on culture, potentially creating positive ontogenetic-evolutionary feedback loops shaping gene–culture coevolution.

Tests of the cultural intelligence hypotheses have been of two main types. Most common have been cross-species, comparative analyses, addressing the prediction that the scale of cultural inheritance in a species will be associated with selection on supportive phenotypic characters. For example, Street et al.63 applied phylogenetic comparative analysis techniques to published databases that span 55 primate genera and 184 species to address relationships between records of social learning and predictor variables. Evidence of greater proclivity for social learning was predicted by both measures of brain size and of reproductive lifespan. The authors concluded that results are ‘consistent with the hypothesis that the evolution of large brains, sociality, and long lifespans has promoted reliance on culture …. in turn driving further increases in brain volume, cognitive abilities, and lifespan in some primate lineages’63.

Culture relies not only on social learning but also on intermittent behavioural innovation, and similar comparative analyses have identified relationships between records of innovation and brain size in both primates64 and birds65. Reinforcing these correlational analyses, a recent mechanistic model of brain evolution concluded that ‘our results are consistent with aspects of various cultural hypotheses for brain evolution’66.

A second approach is to compare closely related species differing in cultural richness, recently explored in a comparison between orangutan species, in which a more extensive cultural repertoire has been described for the Sumatran (Pongo abilii) than for the Bornean species (P. pygmaeus)67. Consistent with the cultural intelligence hypothesis, the Sumatran species have brains reported to be 2–10% larger and showed superior performance in cognitive tests conducted in comparable captive environments67.

Evolutionary effects of culture may explain a further life-history phenomenon, the existence of menopause not only in humans but in whales, where females of matrilineal species may live long after their reproductive span68. Modelling studies have concluded that menopause can evolve through inclusive fitness benefits69. Menopause is predicted to be favoured when females’ relatedness to the group and ability to assist relatives (e.g., by providing a highly competent model from whom to learn) increase with age, but continued reproduction would reduce their capacity to assist relatives69. Older female killer whales are known to be repositories of such extensive adaptive knowledge70.

Correlational tests of the cultural intelligence hypothesis outlined above have, however, been constrained by relatively crude measures of the scope of cultural intelligence in any given species, often resting on post hoc analysis of publications that report non-standardised measures of social learning. In future, the field will benefit from the development of more comparable and systematic variables to be applied in such analyses.

Culture generates selection across species

One difficulty with demonstrating gene–culture coevolution arises when genes and culture are both spread predominantly through transmission from parents to offspring. When culture changes how species interact, however, it can also influence genetic evolution across species boundaries, removing this potential confound. For example, experimental studies with brood parasitic cuckoos and hosts have established that culture may alter the strength of selection across time differently to when culture is absent. Knowledge of the threat of brood parasites (‘cuckoos’) is maintained in groups via social learning among naïve fairy-wren (Malurus cyaneus) hosts71,72, and reed warblers (Acrocephalus scirpaceus) learn about the identity of cuckoos that mimic more dangerous enemies horizontally from peers18,19,73. In reed warblers at least, this socially learned and transmitted information leads to increased detection of cuckoos and strengthens selection against the parasite74. However, common cuckoo (Cuculus canorus) females have a colour polymorphism, likely to be an MC1R variant75, that defeats host culture. Social learning about cuckoos is not generalised across morphs, so knowledge spreads quickly only about the common form. In this case, host culture generates a stronger selective advantage for cuckoos that appear different (i.e., negative frequency dependent selection) than if hosts only learned individually18.

Novel behaviours that spread and are maintained through culture also have the potential to initiate, or intensify, selection on interacting species. For example, recent experiments with great tits show that social transmission of foraging preferences can switch a prey species’ defence strategy from crypsis to aposematism76. Another candidate for interspecies gene–culture coevolution lies in the wide array of complex socially learned foraging techniques of killer whales77. Corkeron and Connor78 suggest that the seasonal migrations of baleen whales to the tropics may function to avoid killer whale predation. Although the details of baleen whale migrations seem socially learned79, the drive to migrate is likely to have a genetic basis that may have been influenced by the predatory cultures of killer whales.

There are many familiar examples where humans are the cultural species; these include the industrial revolution increasing selection for melanic forms of peppered moths (Biston betularia)80, and the rise of agriculture facilitating coevolution of novel pathogens with humans81,82. Although evidence for non-human culture altering selection in other species is at present limited, in theory this could influence any type of interaction where social learning in (at least) one party occurs. For example, previously ‘honest’ foraging bumblebees (Bombus terrestris) learn to rob nectar from flowers by observing others83—if this knowledge transmits across generations84, it could shape pollination efficiency and selection on the plant83. The onset of a new foraging culture could also rapidly shift selection on host microbiomes as they adapt to a novel resource, or influence transmission of microbial communities85. Culture influencing genetic change across species boundaries has great potential to demonstrate how gene–culture coevolution can operate.