Natural selection has driven the recurrent loss of an immunity gene that protects Drosophila against a major natural parasite

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 120; no. 33; p. e2211019120
• Main Authors: Arunkumar, Ramesh, Zhou, Shuyu Olivia, Day, Jonathan P, Bakare, Sherifat, Pitton, Simone, Zhang, Yexin, Hsing, Chi-Yun, O'Boyle, Sinead, Pascual-Gil, Juan, Clark, Belinda, Chandler, Rachael J, Leitão, Alexandre B, Jiggins, Francis M
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 15.08.2023
• Subjects: Alleles; Animals; Biological Sciences; Codons; Drosophila - genetics; Drosophila melanogaster - genetics; Fat body; Fruit flies; Gene deletion; Gene expression; Gene frequency; Host-Parasite Interactions; Immune response; Immune response (cell-mediated); Immune system; Immunity; Infections; Insects; Lectins; Lectins - genetics; Natural populations; Natural selection; Parasites; Population genetics; Populations; Selection, Genetic; Wasps - physiology; melanization; cis-regulatory polymorphism; Leptopilina boulardi; loss of function; C-type lectin
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2211019120

Polymorphisms in immunity genes can have large effects on susceptibility to infection. To understand the origins of this variation, we have investigated the genetic basis of resistance to the parasitoid wasp in We found that increased expression of the gene after infection by parasitic wasps was associated with a faster cellular immune response and greatly increased rates of killing the parasite. encodes a protein that is strongly up-regulated in the fat body after infection and localizes to the surface of the parasite egg. In certain susceptible lines, a deletion upstream of the has largely abolished expression. Other mutations predicted to abolish the function of this gene have arisen recurrently in this gene, with multiple loss-of-expression alleles and premature stop codons segregating in natural populations. The frequency of these alleles varies greatly geographically, and in some southern African populations, natural selection has driven them near to fixation. We conclude that natural selection has favored the repeated loss of an important component of the immune system, suggesting that in some populations, a pleiotropic cost to expression outweighs the benefits of resistance.