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NEWS FEATURE NEWS FEATURE Can animal culture drive evolution? Once the purview of humans, culture has been observed in all sorts of animals. But are these behaviors merely ephemeral fads or can they shape the genes and traits of future generations? Carolyn Beans, Science Writer In Antarctic waters, a group of killer whales makes a Scientists once placed culture squarely in the human wave big enough to knock a seal from its ice floe. domain. But discoveries in recent decades suggest that Meanwhile, in the North Atlantic, another killer whale a wide range of cultural practices—from foraging tactics group blows bubbles and flashes white bellies to and vocal displays to habitat use and play—may influ- herd a school of herrings into a ball. And in the Crozet ence the lives of other animals as well (3). Studies at- Archipelago in the Southern Ocean, still another group tribute additional orca behaviors, such as migration charges at seals on a beach, grasps the prey with their routes and song repertoires, to culture (4). Other re- ’ ’ teeth, and then backs into the water (1). Some research suggests that a finch ssong(5),achimpanzees ’ searchers see these as more than curious behaviors nut cracking (3), and a guppy s foraging route (6) are all manifestations of culture. Between 2012 and 2014, over or YouTube photo ops: they see cultural mores— 100 research groups published work on animal culture introduced into populations and passed to future gener- covering 66 species, according to a recent review (7). ations—that can actually affect animals’ fitness. Now, scientists are exploring whether culture may Killer whales, also known as orcas (Orcinus orca), have shape not only the lives of nonhuman animals but the a geographic range stretching from the Antarctic to the evolution of a species. “Culture affects animals’ lives and Arctic. As a species, their diet includes birds, fish, mam- their survival and their fitness,” says the review’s(7)coau- mals, and reptiles. But as individuals, they typically fall thor, behavioral scientist Andrew Whiten of the University into groups with highly specialized diets and hunting of St Andrews in Scotland. “We’ve learned that’sthecase traditions passed down over generations. Increasingly, to an extent that could hardly have been appreciated half a scientists refer to these learned feeding strategies as cul- century ago.” Based on work in whales, dolphins, and ture, roughly defined as information that affects behavior birds, some researchers contend that animal culture is likely and is passed among individuals and across generations a common mechanism underlying animal evolution. But through social learning, such as teaching or imitation (2). testing this hypothesis remains a monumental challenge. Riding a Cultural Wave Animal populations essentially have two streams of information, genetic and cultural, explains ecologist and whale researcher Hal Whitehead of Dalhousie University in Canada. In the case of the cultural stream, he says, “things are being learned, sometimes from the mother, possibly from the father, as well as from peers and unrelated adults.” Whitehead and others want to understand how these streams interact. Lactose tolerance in humans is a classic example. Studies suggest that adult production of lactase—the enzyme necessary for digesting the sugar lactose in milk—coevolved with the cultural practice of dairy farming in Europe in the last 10,000 years (8). Showing that culture can influence the distribution of genes in an animal population would confirm its role as an evolutionary driver, and Whitehead believes he may have found evidence for exactly that. In the 1990s, Whitehead observed that matrilineal whale species— whose daughters stick with their mothers for life—have Killer whales are divided into groups known as ecotypes, with highly specialized diets and hunting traditions passed down over generations. Here, a low genetic diversity of mitochondrial DNA (9). He “ ” mammal-eating ecotype in the North Pacific hunts seal. Photograph by David coined the term cultural hitchhiking to explain how Ellifrit, courtesy of Center for Whale Research. this pattern might emerge. In these species, cultures 7734–7737 | PNAS | July 25, 2017 | vol. 114 | no. 30 www.pnas.org/cgi/doi/10.1073/pnas.1709475114 Downloaded by guest on October 2, 2021 are passed from mothers to offspring. If a cultural behavior increases a descendant’s chances of survival and reproduction, then this behavior would persist and become more common in the population. The maternal line’s particular mitochondrial DNA haplotype, which also passes directly from mother to offspring, would simultaneously become more common. “The culture is driving and the gene is riding along,” says Whitehead. “There is no particular functional linkage between them.” Whitehead demonstrated through computer models that cultural hitchhiking is a plausible explanation for reduced genetic diversity in matrilineal whale species. Cultural hitchhiking, it seems, is also at work in a population of bottlenose dolphins in western Shark Bay, Western Australia, according to research by evolutionary geneticist Michael Krützen of the University of Zurich (10). In this population, some dolphins carry sponges on their rostrums, most likely for protection as they probe the rough seafloor for fish that they otherwise couldn’t reach (11). This behavior is passed from mothers to offspring through social learning and all “sponging” dolphins in the population share the same mitochondrial haplotype. Because the sponging dolphins primarily inhabit a deep channel where the sponges occur, this culture appears to affect the fine- scale geographic distribution of the mitochondrial genes. “What is really exciting here is that the cultural practice of sponging has led to a change in the genetic For birds in the tanager family, like this magpie tanager (Cissopis leveriana)in make-up of the population when you look at mito- Brazil’s Itatiaia National Park, song is a cultural trait that must be learned. Song chondrial DNA,” says Krützen. evolves faster in this family than in the ovenbird family, whose species have innate song. Image courtesy of Daniel J. Field (University of Bath, Bath, United Kingdom). An Evolutionary Force Longstanding ecological and evolutionary theories distinct hunting strategies as ecotypes, subsets of a suggest that culture could also more directly affect the species that occupy unique ecological niches. New evolution of traits, and even the making of species. genomics technologies allow researchers to search for Animal populations evolve through natural selection evolutionary consequences of these various hunting when a heritable trait, like beak size or fur color, varies cultures. “We came into the genomics era and really and different versions of the trait allow some individuals wanted to see whether these cultural traditions in killer to survive and reproduce more than others. whales led to enough of a long-term selection pressure Animal culture has the potential to affect this process that you would actually see changes in the genome,” in a number of ways, says Whiten. For one, cultural in- says evolutionary biologist Andrew Foote of Bangor novations, such as tools or predator-avoidance tactics, University in the United Kingdom. couldincreaseananimal’s survival and reproduction, Foote and colleagues sequenced the genomes of buffering them against some selection pressures. But 48 orcas across 5 ecotypes to identify whether the culture could also enable animals to colonize regions groups were truly genetically isolated, and whether their they otherwise couldn’t, exposing them to new selec- different cultures were associated with unique genomic tion pressures, such as novel temperatures, predators, changes (1). The sample included one mammal-eating or food sources. And culture could generate selection for animals to be better suited to a cultural behavior and one salmon-eating ecotype from the North Pacific, through physical changes, such as stronger arms for and one mammal-eating, one penguin-eating, and one more powerful hammering, or cognitive ones, such as Antarctic toothfish-eating ecotype from the Antarctic. the ability to learn tool use by mirroring others. “And The researchers found that the groups were genetically “ that, of course, may affect the evolution of the brain to distinct. What is really surprising is just how differenti- match,” says Whiten. Furthermore, cultural differences, ated the ones that live in the same area are,” says Foote. such as birdsong or migration patterns, could prevent “The two North Pacific ones are really different genet- groups from mating together, which could help main- ically even though there is overlap in their range.” tain or even generate new species. Foote estimated that these ecotypes began di- Or anyway, those are the working theories. Finding verging within the last 250,000 years. He traced some definitive evidence is a tricky prospect, though recent of the genetic differences among groups to gene research in whales and birds offers some substantive variants possibly associated with adaptation to the support. Scientists refer to the many orca groups with hunting traditions of each ecotype, and the unique Beans PNAS | July 25, 2017 | vol. 114 | no. 30 | 7735 Downloaded by guest on October 2, 2021 geographic regions those ecotypes colonized. For innate song. Culture, therefore, might actually ramp up example, the two mammal-eating ecotypes were the pace of speciation. each associated with gene variants that play key roles Derryberry and Mason (12) acknowledge that they in regulating the metabolism of methionine, an es- don’t know whether bird song evolution drives speciation sential amino acid that mammal eaters consume in a or vice versa. In one scenario, bird song could diverge first, boom–bust cycle with influxes following each kill. And which would prevent individuals with different songs from the ecotypes that live in the extreme cold of the mating together, setting their lineages on the path to be- Antarctic were associated with gene variants involved coming distinct species.

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