Gene–culture coevolution in whales and dolphins

Abstract

Whales and dolphins (Cetacea) have excellent social learning skills as well as a long and strong mother-calf bond. These features produce stable cultures, and, in some species, sympatric groups with different cultures. There is evidence and speculation that this cultural transmission of behavior has affected gene distributions. Culture seems to have driven killer whales into distinct ecotypes, which may be incipient species or subspecies. There are ecotypespecific signals of selection in functional genes that correspond to cultural foraging behavior and habitat use by the different ecotypes. The five species of whale with matrilineal social systems have remarkably low diversity of mtDNA. Cultural hitchhiking, the transmission of functionally neutral genes in parallel with selective cultural traits, is a plausible hypothesis for this low diversity, especially in sperm whales. In killer whales the ecotype divisions, together with founding bottlenecks, selection, and cultural hitchhiking, likely explain the low mtDNA diversity. Several cetacean species show habitat-specific distributions of mtDNA haplotypes, probably the result of mother-offspring cultural transmission of migration routes or destinations. In bottlenose dolphins, remarkable small-scale differences in haplotype distribution result from maternal cultural transmission of foraging methods, and largescale redistributions of sperm whale cultural clans in the Pacific have likely changed mitochondrial genetic geography. With the acceleration of genomics new results should come fast, but understanding gene-culture coevolution will be hampered by the measured pace of research on the socio-cultural side of cetacean biology.gene-culture coevolution | Cetacea | cultural hitchhiking E volution is dependent on inheritance. Although the transmission of genes is primary, it is not the only mode of inheritance. As recently articulated in the extended evolutionary synthesis, inheritance extends beyond genes to include epigenetic inheritance, physiological inheritance, ecological inheritance, social transmission, and cultural inheritance, all of which can lead to heritability of phenotype (1). From the perspective of modern humans, cultural inheritance, which directly determines much of our own behavior as well as indirectly determining how we affect the global environment, has particular salience (2).Culture, as an inheritance system, can be defined as behavior or information shared within a community that is acquired from conspecifics through some form of social learning (3), i.e., learning that is influenced by observation of, or interaction with, another animal or its products (4). Social learning comes in a range of forms including imitation, emulation, teaching, and local enhancement (5), all of which can promote behavioral similarity between learner and model. Culture may include a wide range of behavior, including foraging methods, vocalizations, diet selection, social behavior, movement, habitat use, social structure, and play (e.g., refs. 3 and 6); potentiall...

Cultural evolutionary theory: How culture evolves and why it matters

“…Cultural transmission also has large-scale evolutionary implications for some nonhuman animals: For example, theoretical studies suggest that nonrandom mating in birds based on culturally transmitted songs could accelerate speciation (180,181) and that sexual selection on learned songs could influence evolution of the neural underpinnings of learning (182). Recently, studies in a range of animal species have shown that cultural practices can emerge, spread, and change over time, potentially influencing individuals' fitness (183)(184)(185)(186)(187). Tool use among chimpanzees and capuchins (188)(189)(190)) is one such example, which also provides insight regarding the possible origins of the early phases of our own species' adaptation to the "cultural niche" (191,192).…”

The extension of biology through culture

“…Hundreds of laboratory experimental studies have demonstrated social learning and transmission in a wide variety of animals. Social learning is now extensively documented in mammals (29), with a particular intensity of research studies in primates (30)(31)(32)(33) and cetaceans (34)(35)(36)(37), in birds (38)(39)(40)(41), in fish (42), and in insects (43,44). The fact that social learning has been shown to play important roles spanning multiple functional contexts (25)(26)(27)(28) suggests that many animals are not simply acquiring one or a few behavioral patterns socially, but rather that social learning is central to their acquisition of adaptive behavior.…”

“…The most comprehensive analyses of such effects in cultural evolution among animals have been in whales and dolphins (34,35). In some species, different migratory routes appear to be culturally transmitted from mothers to calves, thence reflected in diverging genetic make-ups.…”

“…In some species, different migratory routes appear to be culturally transmitted from mothers to calves, thence reflected in diverging genetic make-ups. Most striking is the case of the differentiation of killer whale ecotypes characterized by alternative hunting strategies (targeted at seals vs. salmon and other fish, for example), song types, and residence patterns, that are proposed to be responsible for anatomical changes, such as different jaw types suited to alternative prey (35,98).…”

Can animal culture drive evolution?

“…But discoveries in recent decades suggest that a wide range of cultural practices-from foraging tactics and vocal displays to habitat use and play-may influence the lives of other animals as well (3). Studies attribute additional orca behaviors, such as migration routes and song repertoires, to culture (4). Other research suggests that a finch's song (5), a chimpanzee's nut cracking (3), and a guppy's foraging route (6) are all manifestations of culture.…”