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 awave big enough to knock a seal from its ice floe.Meanwhile, in the North Atlantic, another killer whalegroup blows bubbles and flashes white bellies toherd a school of herrings into a ball. And in the CrozetArchipelago in the Southern Ocean, still another groupcharges at seals on a beach, grasps the prey with theirteeth, and then backs into the water (1). Some re-searchers see these as more than curious behaviorsor YouTube photo ops: they see cultural mores—introduced into populations and passed to future gener-ations—that can actually affect animals’ fitness.

Killer whales, also known as orcas (Orcinus orca), havea geographic range stretching from the Antarctic to theArctic. As a species, their diet includes birds, fish, mam-mals, and reptiles. But as individuals, they typically fallinto groups with highly specialized diets and huntingtraditions passed down over generations. Increasingly,scientists refer to these learned feeding strategies as cul-ture, roughly defined as information that affects behaviorand is passed among individuals and across generationsthrough social learning, such as teaching or imitation (2).

Scientists once placed culture squarely in the humandomain. But discoveries in recent decades suggest thata wide range of cultural practices—from foraging tacticsand vocal displays to habitat use and play—may influ-ence the lives of other animals as well (3). Studies at-tribute additional orca behaviors, such as migrationroutes and song repertoires, to culture (4). Other re-search suggests that a finch’s song (5), a chimpanzee’snut cracking (3), and a guppy’s foraging route (6) are allmanifestations of culture. Between 2012 and 2014, over100 research groups published work on animal culturecovering 66 species, according to a recent review (7).

Now, scientists are exploring whether culture mayshape not only the lives of nonhuman animals but theevolution of a species. “Culture affects animals’ lives andtheir survival and their fitness,” says the review’s (7) coau-thor, behavioral scientist Andrew Whiten of the Universityof St Andrews in Scotland. “We’ve learned that’s the caseto an extent that could hardly have been appreciated half acentury ago.” Based on work in whales, dolphins, andbirds, some researchers contend that animal culture is likelya common mechanism underlying animal evolution. Buttesting this hypothesis remains a monumental challenge.

Riding a Cultural WaveAnimal populations essentially have two streams of in-formation, genetic and cultural, explains ecologist andwhale researcherHalWhiteheadofDalhousie University inCanada. In the case of the cultural stream, he says, “thingsare being learned, sometimes from the mother, possiblyfrom the father, as well as from peers and unrelatedadults.” Whitehead and others want to understand howthese streams interact. Lactose tolerance in humans is aclassic example. Studies suggest that adult production oflactase—the enzyme necessary for digesting the sugarlactose in milk—coevolved with the cultural practice ofdairy farming in Europe in the last 10,000 years (8).

Showing that culture can influence the distributionof genes in an animal population would confirm its roleas an evolutionary driver, and Whitehead believes hemay have found evidence for exactly that. In the 1990s,Whitehead observed that matrilineal whale species—whose daughters stick with their mothers for life—havelow genetic diversity of mitochondrial DNA (9). Hecoined the term “cultural hitchhiking” to explain howthis pattern might emerge. In these species, cultures

Killer whales are divided into groups known as ecotypes, with highly specializeddiets and hunting traditions passed down over generations. Here, amammal-eating ecotype in the North Pacific hunts seal. Photograph by DavidEllifrit, courtesy of Center for Whale Research.

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are passed from mothers to offspring. If a culturalbehavior increases a descendant’s chances of sur-vival and reproduction, then this behavior wouldpersist and becomemore 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 functionallinkage between them.” Whitehead demonstratedthrough computer models that cultural hitchhiking is aplausible explanation for reduced genetic diversity inmatrilineal whale species.

Cultural hitchhiking, it seems, is also at work in apopulation of bottlenose dolphins in western SharkBay, Western Australia, according to research by evo-lutionary geneticist Michael Krützen of the University ofZurich (10). In this population, some dolphins carrysponges on their rostrums, most likely for protection asthey probe the rough seafloor for fish that they other-wise couldn’t reach (11). This behavior is passed frommothers to offspring through social learning and all“sponging” dolphins in the population share the samemitochondrial haplotype. Because the sponging dol-phins primarily inhabit a deep channel where thesponges occur, this culture appears to affect the fine-scale geographic distribution of the mitochondrialgenes. “What is really exciting here is that the culturalpractice of sponging has led to a change in the geneticmake-up of the population when you look at mito-chondrial DNA,” says Krützen.

An Evolutionary ForceLongstanding ecological and evolutionary theoriessuggest that culture could also more directly affect theevolution of traits, and even the making of species.Animal populations evolve through natural selectionwhen a heritable trait, like beak size or fur color, variesand different versions of the trait allow some individualsto survive and reproduce more than others.

Animal culture has the potential to affect this processin a number of ways, says Whiten. For one, cultural in-novations, such as tools or predator-avoidance tactics,could increase an animal’s survival and reproduction,buffering them against some selection pressures. Butculture could also enable animals to colonize regionsthey otherwise couldn’t, exposing them to new selec-tion pressures, such as novel temperatures, predators,or food sources. And culture could generate selectionfor animals to be better suited to a cultural behaviorthrough physical changes, such as stronger arms formore powerful hammering, or cognitive ones, such asthe ability to learn tool use by mirroring others. “Andthat, of course, may affect the evolution of the brain tomatch,” says Whiten. Furthermore, cultural differences,such as birdsong or migration patterns, could preventgroups from mating together, which could help main-tain or even generate new species.

Or anyway, those are the working theories. Findingdefinitive evidence is a tricky prospect, though recentresearch in whales and birds offers some substantivesupport. Scientists refer to the many orca groups with

distinct hunting strategies as ecotypes, subsets of aspecies that occupy unique ecological niches. Newgenomics technologies allow researchers to search forevolutionary consequences of these various huntingcultures. “We came into the genomics era and reallywanted to see whether these cultural traditions in killerwhales led to enough of a long-term selection pressurethat you would actually see changes in the genome,”says evolutionary biologist Andrew Foote of BangorUniversity in the United Kingdom.

Foote and colleagues sequenced the genomes of48 orcas across 5 ecotypes to identify whether thegroupswere truly genetically isolated, andwhether theirdifferent cultures were associated with unique genomicchanges (1). The sample included one mammal-eatingand one salmon-eating ecotype from the North Pacific,and one mammal-eating, one penguin-eating, and oneAntarctic toothfish-eating ecotype from the Antarctic.The researchers found that the groups were geneticallydistinct. “What is really surprising is just how differenti-ated the ones that live in the same area are,” says Foote.“The two North Pacific ones are really different genet-ically even though there is overlap in their range.”

Foote estimated that these ecotypes began di-verging within the last 250,000 years. He traced someof the genetic differences among groups to genevariants possibly associated with adaptation to thehunting traditions of each ecotype, and the unique

For birds in the tanager family, like this magpie tanager (Cissopis leveriana) inBrazil’s Itatiaia National Park, song is a cultural trait that must be learned. Songevolves faster in this family than in the ovenbird family, whose species have innatesong. Image courtesy of Daniel J. Field (University of Bath, Bath, United Kingdom).

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geographic regions those ecotypes colonized. Forexample, the two mammal-eating ecotypes wereeach associated with gene variants that play key rolesin regulating the metabolism of methionine, an es-sential amino acid that mammal eaters consume in aboom–bust cycle with influxes following each kill. Andthe ecotypes that live in the extreme cold of theAntarctic were associated with gene variants involvedin the development of adipose tissue, which couldprotect individuals from the frigid climate.

Foote doesn’t believe the cultural barrier betweenorca ecotypes is long-lasting enough to divide groupsinto different species altogether. “They probably radi-ate and collapse and radiate and collapse,” he says.“Maybe one or two might escape that process and goon to become fully fledged species. But looking at whatwe know now, knowing that they have a relatively re-cent common ancestor, it would suggest that [splittinginto species] never happened in the past.”

Speciation and SongBirdsong, often used to identify mates, offers anotherrobust means for probing culture’s impact on specia-tion and animal evolution. For some bird species, songis innate. For others, it’s essentially cultural, a trait thatmust be learned. In both cases, song evolves over time

as it passes through generations. Evolutionary biologistElizabeth Derryberry of the University of Tennessee,Knoxville, and Nicholas Mason, a doctoral candidate inecology and evolutionary biology at Cornell University,studied two families of birds: the tanagers (Thraupidae)that learn song and the ovenbirds (Furnariidae) that areinnate singers (12). What they found suggests thatculture could play a sizeable role.

Derryberry and Mason analyzed nearly 4,500 songrecordings across nearly 600 species within thesefamilies. For each recording, they measured eightvocal characters, including maximum volume, rangeof pitch, and length. By studying differences in thesecharacters between species in the same family, theresearchers estimated how quickly song evolved indifferent branches of the family tree. If song differedgreatly between closely related species, for example,that would suggest a fast rate of song evolution. Foreach family, they merged this song dataset with agenetic one that showed rates of speciation; the ideawas to identify any connection between the rates ofsong change and species divisions.

Derryberry and Mason found that when the rate ofsong evolution sped up in a branch of a family tree, sotoo did the rate of speciation. But song evolved1.4 times faster in the tanager family, with culturaltransmission of song, than in the ovenbird family, with

innate song. Culture, therefore, might actually ramp upthe pace of speciation.

Derryberry and Mason (12) acknowledge that theydon’t know whether bird song evolution drives speciationor vice versa. In one scenario, bird song could diverge first,which would prevent individuals with different songs frommating together, setting their lineages on the path to be-coming distinct species. Alternatively, the species coulddiverge first by some other mechanism, which would cre-ate strongnatural selection for songdivergence to follow. Ifsong evolution comes first, then the faster bird songevolves, the more rapidly species diverge. “My inkling isthat rapid evolution of birdsong could contribute to spe-ciation,” says Mason. “At the scale we are looking at, welook at patterns, so interpreting process becomes tricky.”

A separate, long-term study may offer insight intothe speciation cause and effect. For four decades,evolutionary biologists Peter and Rosemary Grant ofPrinceton University carefully tracked the survival, mat-ing, and reproduction success of about 12,000 individ-ual birds in species of Darwin’s finches on the island ofDaphne Major in the Galapagos (5). In these species,which belong to the tanager family included in Mason’sstudy, offspring learn song from their fathers.

In 1981, a male bird from a nearby island arrived onDaphne Major singing a song the Grants had neverheard. Genetic analyses (conducted decades later withmicrosatellite data) suggested that it was possibly a hy-brid of the medium ground finch (Geospiza fortis) andthe cactus finch (Geospiza scandens), two species thatwere also found on Daphne Major. But this bird, whichthe Grants call “Big Bird,” was much larger than theparent species. Big Bird survived for 13 years in his newhome and found six mates: the first three hybrids likehimself, the last three all medium ground finches. To-gether with one of the medium ground finches, Big Birdproduced offspring that bred only with one another,resulting in the beginnings of an incipient species thatthe Grants have now followed through six generations.

The bird’s unique song passed on through genera-tions helped members of his lineage recognize one an-other as potential mates. “It’s very important that it’s hadcultural transmission of song,” says Rosemary Grant.There is no agreed upon standard for how many gener-ations a lineage must remain reproductively isolated be-fore it can be called a new species, so the Grants maintainonly that the Big Bird lineage is a species in the making.

Many UnknownsDespite such findings, well-documented examples ofanimal culture influencing evolution remain rare, even inhumans’ closest relatives, primates. There’s little doubtthat cultural differences and social learning are impor-tant to primates’ lives. But can such behaviors have anevolutionary impact?

Whiten cites work supporting an evolutionary ver-sion of the “cultural intelligence hypothesis” in pri-mates: the idea that species with culturally richcommunities will experience selection to enhance thecognitive abilities that support social learning, whichwould in turn require a larger brain capable of pro-cessing learning and storing learned information. This

“My inkling is that rapid evolution of birdsong couldcontribute to speciation.”

—NicholasMason

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larger brain could possibly result in increased overallintelligence. “You may get into a feedback cycle here;as you become more cultural, that selection pressureon the brain and cultural capacities then make youable to become more cultural, which in turn selects forgreater brain size,” says Whiten.

Indeed, a recent study by Kevin Laland, of the Uni-versity of St Andrews, and colleagues found that inprimate species, reliance on social learning is positivelycorrelated with brain volume, as well as social groupsize and lifespan (13). But the authors acknowledge thatthey cannot determine whether selection on sociallearning actually caused the evolution of larger brainsize. It’s also possible that larger brains evolved first forsome other purpose, and then cultural advances madepossible by enhanced cognitive abilities followed.

Whitehead wouldn’t be surprised if researchers findsupport for gene-culture evolution in primates. “There isevidence that some cultural elements in chimpanzeeshave remarkable stability, and stability is a prerequisite forculture having a major effect on genetics.” To find thateffect, he says researchers might test, for example,whether chimpanzee populations with a culture of usingstones as tools also carry gene variants that enhance theirabilities to use those tools, such as greater hand–eye co-ordination or muscle strength in parts of their bodies. Butthe field is still new and such proposals remain theoretical.

Thepaucity of examples could also indicate that animalculture is not quite influential or stable enough to routinelyhave an impact on evolution, says cultural evolutionistPeter Richersonof theUniversity of California,Davis, who ispresident of the recently founded Cultural Evolution So-ciety. “There [are] just more targets in the case of humansthan in the case of other culture-bearing animals,” he says.“That doesn’t mean that wewon’t find a lot of examples—I expect wewill in the long run. But it still ought to bemorespectacular in humans than in other animals.”

Even in humans, thus far there are only a few ex-amples in which potential genetic changes have beenconclusively linked to cultural variation. “The strongcases are where we see independent cultural evolution:dairy farming cropping up multiple places and the

same genes popping up,” says Foote. “That’s missingin most tentative cases.”

One of the biggest challenges with animal studies isdetermining whether genetic differences between pop-ulations are really a response to culture or merely a sig-nature of genetic drift: chance fluctuations in thefrequencies of gene variants over time. “It’s not an easytask. You really need to know something about the de-mographic history of your species,” says Krützen. He callsFoote’s orca ecotypes study amazing, in part because it atleast partially disentangled genetic drift from culturallydriven natural selection. Ideally, Krützen would like to seeevidence that this same gene is under selection in manydifferent species all experiencing a similar selectionpressure. Indeed, Foote notes that adipose tissue genevariants are also under selection in the polar bear whencompared with the brown bear, which may similarly helpbuffer this Arctic animal against a frigid climate (14).

Even once scientists identify genes that may beunder selection, they still must determine whether thegenes connect back to culture. “One of the difficultiesis that there aren’t that many genes that we actuallyknow exactly what they do, even in humans, even less inother species, and certainly in nonmodel species likethe whales,” says Whitehead. The conventional strat-egy for definitively determining a gene–phenotypeconnection entails experimentally altering, for example,a gene in orcas related to adipose tissue, and then re-cording the effects. “But, of course, we can’t do this,”Krützen says. He says that instead, scientists often at-tempt to assign function to a gene by comparing it tosimilar genes of known function in humans. This ap-proach may work well for studying close animal rela-tives like primates. “The farther you go away fromhumans,” he says, “the harder this gets.”

Even while recognizing the research limitations, Krüt-zen remains undeterred. “I’mconvinced that as timegoesby there will be more studies finding more evidence ofgenetic change based on culture,” he says. Foote is lesscertain. “I think a lot of it comes under ‘untested andunknown’,” he says. “Andwe have to keep an openmindas to what the alternative hypotheses are.”

1 Foote AD, et al. (2016) Genome-culture coevolution promotes rapid divergence of killer whale ecotypes. Nat Commun 7:11693.2 Whiten A, Ayala FJ, Feldman MW, Laland KN (2017) The extension of biology through culture. Proc Natl Acad Sci USA 114:7775–7781.3 Whiten A (2017) Culture extends the scope of evolutionary biology in the great apes. Proc Natl Acad Sci USA 114:7790–7797.4 Whitehead H (2017) Gene–culture coevolution in whales and dolphins. Proc Natl Acad Sci USA 114:7814–7821.5 Grant PR, Grant BR (2014) 40 Years of Evolution: Darwin’s Finches on Daphne Major Island (Princeton Univ Press, Princeton, NJ).6 Laland KN, Williams K (1997) Shoaling generates social learning of foraging information in guppies. Anim Behav 53:1161–1169.7 Galef BG, Whiten A (2017) The comparative psychology of social learning. APA Handbook of Comparative Psychology, ed Call J(American Psychological Association, Washington, DC), pp 411–439.

8 Itan Y, Powell A, Beaumont MA, Burger J, Thomas MG (2009) The origins of lactase persistence in Europe. PLOS Comput Biol5:e1000491.

9 Whitehead H (2003) Sperm Whales: Social Evolution in the Ocean (The Univ of Chicago Press, Chicago).10 Kopps AM, et al. (2014) Cultural transmission of tool use combined with habitat specializations leads to fine-scale genetic structure in

bottlenose dolphins. Proc Biol Sci 281:20133245.11 Krützen M, et al. (2014) Cultural transmission of tool use by Indo-Pacific bottlenose dolphins (Tursiops sp.) provides access to a novel

foraging niche. Proc Biol Sci 281:20140374.12 Mason NA, et al. (2017) Song evolution, speciation, and vocal learning in passerine birds. Evolution 71:786–796.13 Street SE, Navarrete AF, Reader SM, Laland KN (2017) Coevolution of cultural intelligence, extended life history, sociality, and brain

size in primates. Proc Natl Acad Sci USA 114:7908–7914.14 Liu S, et al. (2014) Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears. Cell 157:785–794.

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