In memoriam: Jean R. David (1931-2021)
Jean Robert David, the last active member of the French generation who significantly contributed to the establishment of the nine species in the Drosophila melanogaster subgroup as a model for evolutionary genetics, passed away on June 19, 2021, aged 90.
Jean dedicated his 70-year academic career to studying Drosophila biology and evolution, starting as an assistant teacher of biology at the University of Lyon in the early 1950s. His master’s thesis, under the supervision of Victor Nigon (1920–2015), a major figure in the history of Caenorhabditis genetics, concerned the effects of temperature and nutrition on the vestigial mutant in D. melanogaster. There, he made the surprising observation that homozygotes developed the vestigial phenotype when reared on fresh medium; but if reared on old medium (i.e., medium used by larvae from a previous generation) their offspring developed normal wings. This influence of nutrition on the genotype-phenotype map fascinated Jean, and his doctoral work analyzed those effects and their possible transgenerational transmission. Jean’s PhD thesis and subsequent research focused on life history traits (e.g., fecundity, developmental time, longevity, body size, etc.). He believed that fitness effects of genotypes in the laboratory were best understood using optimized media that minimized dietary effects. After testing the effects of a plethora of nutritional elements and food conditions, he developed a standard axenic medium that remains among the most widely used. Following a short postdoc in Edinburgh (Scotland) with Forbes W. Robertson (1920-2012) on Drosophila quantitative genetics, Jean returned to Lyon, where he assumed a professorship position. His laboratory studied environmental effects on phenotypic variation, focusing on the physiology of egg production, food intake, and oviposition-site choice.
Although Jean was a passionate naturalist with a keen interest in insects (he described a new beetle species from the Saone valley in 1963 and a new earwig subspecies from Mont Mézenc in 1973), his work on Drosophila in Lyon was limited to a few laboratory strains. An encounter with researchers from Gif-sur-Yvette, in particular Charles Bocquet (1921-1977) and Léonidas Tsacas (1923-2016), profoundly changed his career and research interests. In the late 1960s, Tsacas secured a major grant to study Afrotropical drosophilids. He invited many French scientists to participate, including Jean who spent one month in Gabon in July 1970. This turned out to be a life-changing experience. First, he realized that Afrotropical D. melanogaster differed in multiple morphological, physiological, and behavioral aspects from worldwide, temperate populations. Second, he became aware of the great taxonomic and ecological diversity of Afrotropical species. Both observations tightened Jean’s collaborations with the Gif laboratory. With Bocquet, he demonstrated in a Nature paper the significant genetic and phenotypic variability among natural populations of D. melanogaster and its sibling species D. simulans, a variation that had not been seen when only non-African populations were studied. For morphological traits like body size, the variability showed parallel latitudinal clines between the two species, likely due to convergent adaptation to cold climate. For other traits such as alcohol tolerance, however, only D. melanogaster populations showed clinal variation with Northern flies being more adapted to highly fermenting resources. Temperature and alcohol became the two main environmental factors that Jean would focus on in subsequent experimental studies.
Jean quickly went from one field expedition to another, collecting flies on islands as remote as Guadeloupe, Martinique, La Réunion, Mauritius, and Seychelles, and also in Singapore and several African countries. He and Tsacas maintained a strong collaboration by sharing the flies they collected. At the beginning of Tsacas’ project, only three species of the melanogaster subgroup were known: D. melanogaster, D. simulans, and D. yakuba, with melanogaster and simulans cosmopolitan and yakuba endemic to Africa. In 1971, Tsacas described a fourth species from Zimbabwe, D. teissieri; and in the same year, his PhD student Daniel Lachaise (1947-2006) discovered a fifth species from Côte d’Ivoire, D. erecta. Crosses between all those species were impossible or very difficult. In 1973, Jean discovered a sixth species, D. mauritiana, from the island of Mauritius. Unlike the previous species, D. mauritiana readily crossed with D. simulans, producing sterile hybrid males but fertile females. Its close relation to both D. simulans and D. melanogaster made it ideal for studying the genetic basis of speciation in the subgroup. In 1975, Tsacas, Lachaise, and Jean made a joint expedition to Cameroon that led to the discovery of a seventh species of the subgroup, D. orena. Those findings established the Afrotropical origin of the melanogaster species subgroup and pioneered the clade as a premier model for evolutionary genetics.
Following Bocquet’s death in 1977, Jean resigned from the University of Lyon and became the director of the Gif laboratory. Under his directorship, the laboratory continued the study of the evolutionary genetics of the melanogaster subgroup. The 1980s saw two main findings. First, through the application of more advanced biochemical and molecular tools, the dispersal routes of D. melanogaster became clearer. In addition to reconfirming the “out-of-Africa” hypothesis, these biochemical markers helped Jean demonstrate that alcohol-resistant D. melanogaster in Congolese breweries were in fact European flies recently introduced to Africa by man. The European-derived Congolese flies showed signals of reproductive isolation from native African flies, representing one of the most intriguing cases of incipient speciation in Drosophila. A second major finding of this period was the discovery of the specialization of D. sechellia, the eighth species of the melanogaster subgroup, on toxic noni fruits on the Seychelles archipelago. Jean had explored those islands in 1977 but did not pay attention to the smelly noni fruits and their hovering drosophilids. Yet, two students from Oxford did, and their collected flies preserved in alcohol were described by Tsacas and Gerhard Bächli in 1981. In the same year, Jean went to the Seychelles, established the first laboratory culture of D. sechellia, and after 10 years of intensive research, he described in a PNAS paper the genetic basis of D. sechellia behavioral and physiological adaptations to noni.
In 1997, Jean retired but continued to work as an emeritus researcher at Gif. Early in this period, he revisited the role of the environment on phenotypic variation but now within a broader evolutionary perspective, comparing the shape of thermal reaction norms for many morphometrical and physiological traits, such as cold tolerance, at both intra- and interspecific scales. This research program produced a wealth of data documenting genetic variability in phenotypic plasticity, a now-popular topic that was then understudied. It required maintaining a large collection of strains that Jean carefully preserved and enriched through continuous fieldwork. His meticulous observation and isolation of the slight phenotypic abnormalities led him to collaborate with several young talented evo-devo researchers unraveling the genetic basis of natural variants. For example, the observation of supernumerary macrochaetes on the back of some D. melanogaster from Morocco led to the identification of a new repressor of the achaete and scute genes. Similarly, describing the loss of a pair of genital bristles between D. yakuba and D. santomea (the ninth species of the melanogaster subgroup, discovered by Lachaise in 1998) identified a single regulatory mutation of scute with a strong pleiotropic effect on multiple sensory targets involved in copulation. In both cases, Jean’s openness and willingness to share his observations led to new discoveries.
Jean also had an interest in investigating species not previously studied. He pioneered analyses of the Afrotropical genus Zaprionus and closely monitored the invasion of Brazil by Z. indianus. He created strong ties with Brazilian drosophilists and was frequently an invited guest at the annual Drosophila conference in Brazil. Following Lachaise’s unexpected death in 2006, Jean preserved the laboratory’s tradition of exploring the African fauna, mostly focusing on Madagascar and its surrounding islands. On the island of Mayotte in 2013, at age 82, he made the last major taxonomic discovery in the melanogaster subgroup. He found a subspecies of D. yakuba specializing on the toxic fruits of noni, like D. sechellia. Again, Jean shared his discovery with young population genomicists. This led to detecting a signal of parallel genetic changes between two distantly related species specializing on the same host.
Jean kept working on his experiments in the laboratory at Gif until he fell ill in October 2020. Reflecting on his long career during his terminal illness, he remembered how reading Jean-Henri Fabre’s (1823-1915) 10-volume Souvenirs entomologiques when he was a teenager influenced his view of the living world. Like Fabre, Jean was an “inimitable observer” who mixed a passion for fieldwork with rigorous laboratory experimentation. He was a prolific writer, publishing more than 400 papers, mostly on drosophilids. His style emphasized clarity, using simple words and statistical tests rather than obscure and complex ones, and avoided unwarranted generalizations and fashionable hypotheses. An avid traveler, talented cook (his fruit tarts and chimney-made grills were unrivalled), warm host, and empathic listener, Jean combined an intellectual aura with a genuinely down-to-earth personality—a rare and wonderful combination.
Jean is survived by his beloved wife, eminent developmental biologist Nicole Le Douarin, two daughters, three grandchildren, and two great-grandchildren.
About the Authors:
Amir Yassin – Laboratoire Evolution, Génomes, Comportement et Ecologie (EGCE), CNRS, IRD, Université Paris-Saclay, Gif-sur-Yvette, France
Patricia Gibert – Laboratoire de Biométrie et Biologie Evolutive (LBBE), CNRS, Université Lyon 1, Villeurbanne, France
Pierre Capy – Laboratoire Evolution, Génomes, Comportement et Ecologie (EGCE), CNRS, IRD, Université Paris-Saclay, Gif-sur-Yvette, France