Natural courtship song variation caused by an intronic retroelement in an ion channel gene

• Published in: Nature (London) 2016-08, Vol.536 (7616), p.329-332
• Main Authors: Ding, Yun, Berrocal, Augusto, Morita, Tomoko, Longden, Kit D., Stern, David L.
• Format: Article
• Language: English
• Subjects: 42/41; 45/43; 45/47; 631/181/2474; 631/208/1515; 64/24; Analysis; Animal behavior; Animal Communication; Animal species; Animals; Base Sequence; Courtship; Drosophila; Drosophila - genetics; Drosophila - physiology; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; Female; Genes; Genetic aspects; Genetic variation; Humanities and Social Sciences; Insects; Introns - genetics; Large-Conductance Calcium-Activated Potassium Channels - genetics; Large-Conductance Calcium-Activated Potassium Channels - metabolism; letter; Male; Males; multidisciplinary; Mutation; Quantitative Trait Loci - genetics; Retroelements - genetics; RNA Splicing; Science; Sexual Behavior, Animal - physiology
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature19093

Natural variation in the courtship song of Drosophila is mapped to the intronic insertion of a retroelement at the slowpoke locus, which encodes an ion channel. On a wing and a song An important aspect of courtship behaviour in Drosophila is the male courtship song, generated when the males vibrate their wings. The features of this courtship song and how this varies between Drosophila species have been well-characterized. David Stern and colleagues now map the genetic variation causal for natural variation in courtship song between two wild isolates of D. simulans and D. mauritiana to the insertion of a retroelement at the slowpoke ( slo ) locus, which encodes an ion channel. Animal species display enormous variation for innate behaviours, but little is known about how this diversity arose. Here, using an unbiased genetic approach, we map a courtship song difference between wild isolates of Drosophila simulans and Drosophila mauritiana to a 966 base pair region within the slowpoke ( slo ) locus, which encodes a calcium-activated potassium channel 1 . Using the reciprocal hemizygosity test 2 , we confirm that slo is the causal locus and resolve the causal mutation to the evolutionarily recent insertion of a retroelement in a slo intron within D. simulans . Targeted deletion of this retroelement reverts the song phenotype and alters slo splicing. Like many ion channel genes, slo is expressed widely in the nervous system and influences a variety of behaviours 3 , 4 ; slo -null males sing little song with severely disrupted features. By contrast, the natural variant of slo alters a specific component of courtship song, illustrating that regulatory evolution of a highly pleiotropic ion channel gene can cause modular changes in behaviour.