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Can culture drive evolution? Once the purview of humans, culture has been observed in all sorts of . But are these behaviors merely ephemeral fads or can they shape the genes and traits of future generations?

Carolyn Beans, Science Writer

In 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 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 , 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 re- search 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 , 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 , 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 in- formation, 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 sur- vival and reproduction, then this behavior would persist and become more common in the population. The maternal line’s particular mitochondrial DNA hap- lotype, which also passes directly from mother to off- spring, 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 Bay, Western Australia, according to research by evo- lutionary geneticist Michael Krützen of the University of Zurich (10). In this population, some dolphins carry on their rostrums, most likely for protection as they probe the rough seafloor for fish that they other- wise 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 dol- phins 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 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 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. Alternatively, the species could in the development of adipose tissue, which could diverge first by some other mechanism, which would cre- protect individuals from the frigid climate. ate strong natural selection for song divergence to follow. If Foote doesn’t believe the cultural barrier between song evolution comes first, then the faster bird song “ orca ecotypes is long-lasting enough to divide groups evolves, the more rapidly species diverge. My inkling is into different species altogether. “They probably radi- that rapid evolution of birdsong could contribute to spe- ” “ ate and collapse and radiate and collapse,” he says. ciation, says Mason. At the scale we are looking at, we ” “Maybe one or two might escape that process and go look at patterns, so interpreting process becomes tricky. on to become fully fledged species. But looking at what A separate, long-term study may offer insight into we know now, knowing that they have a relatively re- the speciation cause and effect. For four decades, evolutionary biologists Peter and Rosemary Grant of cent common ancestor, it would suggest that [splitting Princeton University carefully tracked the survival, mat- into species] never happened in the past.” ing, and reproduction success of about 12,000 individ- ’ Speciation and Song ual birds in species of Darwin s finches on the island of Daphne Major in the Gal´apagos (5). In these species, Birdsong, often used to identify mates, offers another which belong to the tanager family included in Mason’s robust means for probing culture’simpactonspecia- study, offspring learn song from their fathers. tion and animal evolution. For some bird species, song In 1981, a male bird from a nearby island arrived on is innate. For others, it’s essentially cultural, a trait that Daphne Major singing a song the Grants had never must be learned. In both cases, song evolves over time heard. Genetic analyses (conducted decades later with microsatellite data) suggested that it was possibly a hy- “My inkling is that rapid evolution of birdsong could brid of the medium ground finch (Geospiza fortis)and contribute to speciation.” the cactus finch (Geospiza scandens), two species that — were also found on Daphne Major. But this bird, which Nicholas Mason the Grants call “Big Bird,” wasmuchlargerthanthe parentspecies.BigBirdsurvivedfor13yearsinhisnew as it passes through generations. Evolutionary biologist home and found six mates: the first three hybrids like Elizabeth Derryberry of the University of Tennessee, himself, the last three all medium ground finches. To- Knoxville, and Nicholas Mason, a doctoral candidate in gether with one of the medium ground finches, Big Bird ecology and evolutionary biology at Cornell University, produced offspring that bred only with one another, resulting in the beginnings of an incipient species that studied two families of birds: the (Thraupidae) the Grants have now followed through six generations. that learn song and the ovenbirds (Furnariidae) that are The bird’s unique song passed on through genera- innate singers (12). What they found suggests that tions helped members of his lineage recognize one an- culture could play a sizeable role. other as potential mates. “It’s very important that it’shad Derryberry and Mason analyzed nearly 4,500 song cultural transmission of song,” says Rosemary Grant. recordings across nearly 600 species within these There is no agreed upon standard for how many gener- families. For each recording, they measured eight ations a lineage must remain reproductively isolated be- vocal characters, including maximum volume, range fore it can be called a new species, so the Grants maintain of pitch, and length. By studying differences in these only that the Big Bird lineage is a species in the making. characters between species in the same family, the researchers estimated how quickly song evolved in Many Unknowns different branches of the family tree. If song differed Despite such findings, well-documented examples of greatly between closely related species, for example, animal culture influencing evolution remain rare, even in ’ ’ that would suggest a fast rate of song evolution. For humans closest relatives, primates. There slittledoubt that cultural differences and social learning are impor- each family, they merged this song dataset with a tant to primates’ lives. But can such behaviors have an genetic one that showed rates of speciation; the idea evolutionary impact? was to identify any connection between the rates of Whiten cites work supporting an evolutionary ver- song change and species divisions. sion of the “cultural intelligence hypothesis” in pri- Derryberry and Mason found that when the rate of mates: the idea that species with culturally rich song evolution sped up in a branch of a family tree, so communities will experience selection to enhance the too did the rate of speciation. But song evolved cognitive abilities that support social learning, which 1.4 times faster in the tanager family, with cultural would in turn require a larger brain capable of pro- transmission of song, than in the ovenbird family, with cessing learning and storing learned information. This

7736 | www.pnas.org/cgi/doi/10.1073/pnas.1709475114 Beans Downloaded by guest on October 2, 2021 larger brain could possibly result in increased overall same genes popping up,” says Foote. “That’s missing intelligence. “You may get into a feedback cycle here; in most tentative cases.” as you become more cultural, that selection pressure One of the biggest challenges with animal studies is on the brain and cultural capacities then make you determining whether genetic differences between pop- able to become more cultural, which in turn selects for ulations are really a response to culture or merely a sig- greater brain size,” says Whiten. nature of genetic drift: chance fluctuations in the Indeed, a recent study by Kevin Laland, of the Uni- frequencies of gene variants over time. “It’snotaneasy versity of St Andrews, and colleagues found that in task. You really need to know something about the de- primate species, reliance on social learning is positively mographic history of your species,” says Krützen. He calls correlated with brain volume, as well as social group Foote’s orca ecotypes study amazing, in part because it at size and lifespan (13). But the authors acknowledge that least partially disentangled genetic drift from culturally they cannot determine whether selection on social driven natural selection. Ideally, Krützen would like to see learning actually caused the evolution of larger brain evidence that this same gene is under selection in many size. It’s also possible that larger brains evolved first for different species all experiencing a similar selection some other purpose, and then cultural advances made pressure. Indeed, Foote notes that adipose tissue gene possible by enhanced cognitive abilities followed. variants are also under selection in the polar bear when Whitehead wouldn’t be surprised if researchers find compared with the brown bear, which may similarly help support for gene-culture evolution in primates. “There is buffer this Arctic animal against a frigid climate (14). evidence that some cultural elements in chimpanzees Even once scientists identify genes that may be have remarkable stability, and stability is a prerequisite for under selection, they still must determine whether the culture having a major effect on genetics.” To find that genes connect back to culture. “One of the difficulties effect, he says researchers might test, for example, is that there aren’t that many genes that we actually whether chimpanzee populations with a culture of using know exactly what they do, even in humans, even less in stones as tools also carry gene variants that enhance their other species, and certainly in nonmodel species like abilities to use those tools, such as greater hand–eye co- the whales,” says Whitehead. The conventional strat- ordination or muscle strength in parts of their bodies. But egy for definitively determining a gene–phenotype the field is still new and such proposals remain theoretical. connection entails experimentally altering, for example, The paucity of examples could also indicate that animal a gene in orcas related to adipose tissue, and then re- culture is not quite influential or stable enough to routinely cording the effects. “But, of course, we can’tdothis,” have an impact on evolution, says cultural evolutionist Krützen says. He says that instead, scientists often at- Peter Richerson of the University of California, Davis, who is tempt to assign function to a gene by comparing it to president of the recently founded Cultural Evolution So- similar genes of known function in humans. This ap- ciety. “There [are] just more targets in the case of humans proach may work well for studying close animal rela- than in the case of other culture-bearing animals,” he says. tives like primates. “The farther you go away from “That doesn’t mean that we won’t find a lot of examples— humans,” he says, “the harder this gets.” I expect we will in the long run. But it still ought to be more Even while recognizing the research limitations, Krüt- spectacular in humans than in other animals.” zen remains undeterred. “I’m convinced that as time goes Even in humans, thus far there are only a few ex- bytherewillbemorestudiesfindingmoreevidenceof amples in which potential genetic changes have been genetic change based on culture,” he says. Foote is less conclusively linked to cultural variation. “The strong certain. “I think a lot of it comes under ‘untested and cases are where we see independent cultural evolution: unknown’,” he says. “And we have to keep an open mind dairy farming cropping up multiple places and the as to what the alternative hypotheses are.”

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