A New Frontiers project shows that the tiny fruit fly is able to culturally convey sexual preferences

An interdisciplinary consortium led by TULIP researchers shows that the tiny fruit fly (or Drosophila melanogaster) has the cognitive abilities to culturally transmit its sexual preferences between generations potentially leading to the emergence of cultural traditions of sexual preferences that can potentially persist over thousands of generations. That study published in the renowned journal Science provides the first experimental toolbox to study animal culture in any species, and suggests that the cultural process likely participated to the evolution of a vastly broader spectrum of species and over periods much longer than ever envisioned.

An abundant theoretical literature shows that cultural transmission can considerably change the evolutionary fate of populations. Although the cultural process is often considered as unique to humans, the existence in primates and birds of persistent behavioral variations not reducible to genetic or ecological variation strongly suggests the existence of an animal cultural transmission.

TULIP researchers have formed an interdisciplinary research consortium to dissect the mechanisms leading to cultural transmission in order to test the existence of cultural processes elsewhere than in primates and birds. Their results were published in the journal Science on November 30, 2018

A good example of interdisciplinarity in Toulouse

The consortium for this study is eminently interdisciplinary. It associates two behavioral ecologists from the Evolution & Biological Diversity laboratory (Étienne Danchin and Sabine Nöbel, EDB, CNRS / University Toulouse III Paul Sabatier / IRD), with a neurobiologist at the Research Center on Animal Cognition (Guillaume Isabel , CRCA, CNRS / Univ Toulouse III Paul Sabatier), as well as an international collaborator (Arnaud Pocheville, Autralia, who will soon join EDB on a CNRS position) and several national and international master 2 students.

It is a TULIP New Frontiers project in 2012 that allowed the initiation of this project. It then had a strong leverage effect by obtaining a European Prestige Marie Curie scholarship 2014, two ANR projects in 2013 and 2018 as well as support from LabEx IAST, which is strongly concerned by the question of the origin of social learning and the cultural process, all within the Federal University of Toulouse which also supported with an IDEX Interface Project in 2015

Social learning and cultural transmission between generations

In this study, researchers proposed and applied to the fruit fly a definition of animal culture focusing on the mechanisms of social transmission rather than on patterns of behavioral variation as it was mainly the case in the past. This definition requires that the five criteria discussed in the literature on animal culture to be met simultaneously. The first of them is that the traits be learned socially, i.e. learned from conspecifics. Following the observation of a Drosophila female (called demonstrator female) choosing between a male of type A and a male of type B for mating, an observer female then shows a significant preference (i.e. statistical bias) for males of the type chosen during the demonstration. It is a form of observational social learning called mate-copying.

Based on these remarkable results for a tiny fly weighing less than one milligram, researchers show, in a series of five experiments, that social learning of sexual preferences meets all the criteria leading to state that these preferences can be transmitted culturally across generations. Drosophila female sexual preferences for a male type can be learned socially (criterion 1), from older individuals (criterion 2), and memorized over the long term (criterion 3), in favor of any male of the same type (criterion 4), and in a highly conformist way (criterion 5). For the latter criterion, researchers designed a new device (Photo) in hexagon with six peripheral compartments where six demonstrator females chose between two males (one of each phenotype), around a central arena where observers females could watch them.

Flies are conformist

The very surprising result was that, after the simultaneous observation of the choices of six demonstrator females, observer females showed the same level of preference for males of the type that had been chosen by the demonstrators, regardless of the level of majority for one type among demonstrators (the majority varied from 100% down to only 60% in these experiments). Thus, flies are highly conformist.

Illustration_Science_Danchin_2018

Situation de copie du partenaire dans laquelle deux femelles regardent un mâle vert s'accoupler tandis qu'un mâle rose est rejeté. © David Duneau

Computer simulations then showed that these cognitive characteristics can lead to the emergence of long-lasting cultural traditions along transmission chains in which observers (pupils) of one-step became the demonstrators (teachers) of the next step, and so on. Tey found that conformity plays a key role in the emergence of cultural traditions. Finally, in an experimental transmission chain involving six observer females chains lasted much than predicted in the absence of social learning, but were perfectly predicted by a simulation model reproducing such chains, whic validated their model.They then used that validated model to explore the extent to which the documented social learning capacity could foster the emergence of persistent local traditions of preferring a given male phenotype within a population. They found that in conditions that exist in nature, the social learning of Drosophila does generate long lasting cultural traditions  that sometimes were maintained over at least 100,000 transmission step and potentially spanning over thousands of drosophila generations. An unbelievably long transmission chain.

Drosophila thus have all the cognitive abilities generate long-lasting cultural traditions of preferringa given male phenotype over another. As a result, this insect, which shared it last common ancestor with humans nearly 700 million years ago, have the ability to culturally transmit their sexual preferences across generations, greatly expanding the taxonomic spectrum of the cultural process, and suggesting that, contrary to the usual belief, cultural inheritance has affected the evolution of a very large number of animal species over extended periods of time.

See also

E. Danchin, S. Nöbel, A. Pocheville, A.-C. Dagaeff, L. Demay, M. Alphand, S. Ranty-Roby, L. van Renssen, M. Monier, E. Gazagne, M. Allain & G. Isabel. Cultural flies: conformist social learning in fruit flies predicts long-lasting mate-choice traditions.  Science 362 : 1025-1030. 30 novembre 2018.

Modification date : 07 June 2023 | Publication date : 06 December 2018 | Redactor : Etienne Danchin & Guillaume Cassiède-Berjon