The genome of the bee louse fly reveals deep convergences in the evolution of social inquilinism

Author:

Legout Hélène,Ogereau DavidORCID,Carcaud JulieORCID,Filée Jonathan,Garnery Lionel,Gilbert ClémentORCID,Requier FabriceORCID,Sandoz Jean-ChristopheORCID,Yassin AmirORCID,Bastide HéloïseORCID

Abstract

AbstractThe nests of social insects often harbor a rich fauna of intruders, known as inquilines. Close relatedness between the host and the inquiline prevails due to potential genetic predispositions but how phylogenetically distant inquilines adapt to their hosts remains unclear. Here, we analyzed the genome of the wingless and blind bee louse flyBraula coeca, an inquiline of the Western honey beeApis mellifera. We found that unlike many parasites, such as the human louse, the bee louse genome did not show significant erosion or strict reliance on an endosymbiont, likely due to a relatively recent age of inquilinism. However, a strikingly parallel evolution in a set of gene families was observed between the honey bee and the bee louse. Convergences included genes potentially involved in metabolism and immunity, and the loss of nearly all bitter-tasting gustatory receptors in agreement with life in a protective hive and a major diet of honey, pollens, and beeswax. Vision-related and odorant receptor genes also exhibited rapid losses. Only genes whose orthologs in the closely relatedDrosophila melanogasterrespond to components of the honey bee alarm pheromones or floral aroma were retained, whereas the losses included orthologous receptors responsive to the anti-ovarian honey bee queen pheromone. These results establish a new model for the study of major morphological and neuroethological transitions and indicate that deep genetic convergences between phylogenetically distant organisms can underlie the evolution of social inquilinism.

Publisher

Cold Spring Harbor Laboratory

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