The burgeoning reach of animal culture thumbnail

The burgeoning reach of animal culture

We are not alone

Before the mid-20th century, it was generally assumed that culture, behavior learned from others, was specific to humans. However, starting with identification in a few species, evidence that animals can learn and transmit behaviors has accumulated at an ever-increasing pace. Today, there is no doubt that culture is widespread among animal species, both vertebrates and invertebrates, marine and terrestrial. Whiten reviews evidence for animal culture and elaborates on the wide array of forms that such culture takes. Recognizing that other species have complex and varied culture has implications for conservation and welfare and for understanding the evolution of this essential component of animal societies, including our own.

Science, this issue p. eabe6514

Structured Abstract

BACKGROUND

Culture—the inheritance of an array of behavioral traditions through social learning from others—was once thought specific to humans. Recent and accumulating evidence has shown that, to the contrary, culture permeates the lives of a great diversity of animals, with far-reaching implications for evolutionary biology, anthropology, and conservation. Early evidence for animal culture emerged in the mid–20th century in the discovery of regional birdsong dialects and the spread of provisioned sweet potato washing in Japanese monkeys. Stimulated by these discoveries, long-term studies of wild chimpanzees and orangutans later in the century revealed complex cultures composed of multiple traditions spanning diverse aspects of apes’ lives, from tool use to social and sexual behavior.

In part through the accumulation of further long-term field studies, the present century has witnessed an explosion in discoveries about social learning and culture, not only in primates but also in a rapidly growing range of animal species, from cetaceans to a diverse array of birds, fish, and even invertebrates.

ADVANCES

Novel experimental designs have rigorously demonstrated the cultural transmission and spread of behavioral innovations introduced by researchers, both in the wild and in labs. New statistical methods have detected the signatures of behavioral innovations as they spread through social networks, identifying culture in species (e.g., whales) for which experiments are impractical. Through these and other methodological advances, the reach of cultural learning is now known to encompass an unexpected range of species, with surprising new discoveries extending even to insects, from bees to fruit flies.

The reach of culture has similarly been discovered to span diversity in behavioral domains, including foraging techniques, tool use, vocal communication, social customs and preferences for particular prey, migratory pathways, nesting sites, and mates. The revelation that cultural inheritance permeates many species’ lives is increasingly recognized to have profound implications for evolutionary biology at large, because it provides a second form of inheritance that builds on the primary genetic inheritance system, facilitating cultural evolution. The two inheritance systems may generate rich interactive effects, as they have in humans.

A plethora of innovative experiments has further identified an array of cognitive processes involved in learning from others, ranging from simple and ubiquitous forms to specialized ones such as imitation and teaching. These forms of social learning have been shown to be further refined through a variety of selective biases, such as conforming to majorities or copying particularly skilled elders.

OUTLOOK

United Nations bodies operating under the aegis of international conventions have recently recognized the importance of all that has been discovered about animal cultures, for conservation policies and practices. Among sperm whales and chimpanzees, specific cultural entities, as opposed to genetically defined units, have been recognized as meriting conservation in their own right. This finding, in turn, urges a greater focus on understanding cultural phenomena in the wild. The task of rigorously identifying social learning has relied heavily on controlled experiments in captivity, but field experiments are increasingly carried out. These and other innovative methods to identify and trace animal cultures in the wild deserve to be developed and applied further to wild populations.

The wealth of methodological advances and empirical discoveries about animal cultures in the present century provides an exciting foundation from which to explore deeper questions. Do animal cultures evolve, cumulatively, as human cultures have done so impressively over past millennia? How profoundly does the lifetime reach of culture in animals’ lives reshape our understanding of behavioral ecology and the fundamentals of evolution at large? How close are human and animal cultures now perceived to be, and where do the principal differences remain?

Diversity in cultural species and behavioral domains.

(A) After filial imprinting on the costumed human pilot of a microlight aircraft, young cranes followed the flight path of this surrogate parent, adopting it as a traditional migratory route. (B) Female fruit flies (left) that witness a male marked with one of two colors mating (top right) later prefer to mate with similarly colored males. This behavior is further copied by others, initiating a tradition. (C) Bighorn sheep translocated to unfamiliar locations were initially sedentary, but spring migration and skill in reaching higher-altitude grazing grounds expanded over decades, implicating intergenerational cultural transmission. (D) Groups of vervet monkeys were trained to avoid bitter-tasting corn of one color and to prefer the other. Later, when offered these options with no distasteful additive, both naïve infants and immigrating adult males adopted the experimentally created local group preference. (E) Young meerkats learn scorpion predation because adults initially supply live prey with stingers removed and later provide unmodified prey as the young meerkats mature. (F) A humpback whale innovation of slapping the sea surface to refine predation, known as “lobtail feeding,” spread over two decades to create a new tradition in hundreds of other humpbacks. For reference citations, see the full article.

Photos: (A) Thomas Mueller, (B) Etienne Danchin, (C) istock.com/skibreck, (D) Erica van de Waal, (E) Alex Thornton, (F) Jennifer Allen

” data-hide-link-title=”0″ data-icon-position=”” href=”https://science.sciencemag.org/content/sci/372/6537/eabe6514/F1.large.jpg?width=800&height=600&carousel=1″ rel=”gallery-fragment-images-617253751″ title=”Diversity in cultural species and behavioral domains. (A) After filial imprinting on the costumed human pilot of a microlight aircraft, young cranes followed the flight path of this surrogate parent, adopting it as a traditional migratory route. (B) Female fruit flies (left) that witness a male marked with one of two colors mating (top right) later prefer to mate with similarly colored males. This behavior is further copied by others, initiating a tradition. (C) Bighorn sheep translocated to unfamiliar locations were initially sedentary, but spring migration and skill in reaching higher-altitude grazing grounds expanded over decades, implicating intergenerational cultural transmission. (D) Groups of vervet monkeys were trained to avoid bitter-tasting corn of one color and to prefer the other. Later, when offered these options with no distasteful additive, both naïve infants and immigrating adult males adopted the experimentally created local group preference. (E) Young meerkats learn scorpion predation because adults initially supply live prey with stingers removed and later provide unmodified prey as the young meerkats mature. (F) A humpback whale innovation of slapping the sea surface to refine predation, known as “lobtail feeding,” spread over two decades to create a new tradition in hundreds of other humpbacks. For reference citations, see the full article.”>

Diversity in cultural species and behavioral domains.

(A) After filial imprinting on the costumed human pilot of a microlight aircraft, young cranes followed the flight path of this surrogate parent, adopting it as a traditional migratory route. (B) Female fruit flies (left) that witness a male marked with one of two colors mating (top right) later prefer to mate with similarly colored males. This behavior is further copied by others, initiating a tradition. (C) Bighorn sheep translocated to unfamiliar locations were initially sedentary, but spring migration and skill in reaching higher-altitude grazing grounds expanded over decades, implicating intergenerational cultural transmission. (D) Groups of vervet monkeys were trained to avoid bitter-tasting corn of one color and to prefer the other. Later, when offered these options with no distasteful additive, both naïve infants and immigrating adult males adopted the experimentally created local group preference. (E) Young meerkats learn scorpion predation because adults initially supply live prey with stingers removed and later provide unmodified prey as the young meerkats mature. (F) A humpback whale innovation of slapping the sea surface to refine predation, known as “lobtail feeding,” spread over two decades to create a new tradition in hundreds of other humpbacks. For reference citations, see the full article.

Photos: (A) Thomas Mueller, (B) Etienne Danchin, (C) istock.com/skibreck, (D) Erica van de Waal, (E) Alex Thornton, (F) Jennifer Allen

Abstract

Culture can be defined as all that is learned from others and is repeatedly transmitted in this way, forming traditions that may be inherited by successive generations. This cultural form of inheritance was once thought specific to humans, but research over the past 70 years has instead revealed it to be widespread in nature, permeating the lives of a diversity of animals, including all major classes of vertebrates. Recent studies suggest that culture’s reach may extend also to invertebrates—notably, insects. In the present century, the reach of animal culture has been found to extend across many different behavioral domains and to rest on a suite of social learning processes facilitated by a variety of selective biases that enhance the efficiency and adaptiveness of learning. Far-reaching implications, for disciplines from evolutionary biology to anthropology and conservation policies, are increasingly being explored.

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