title: Evolution of Drosophila sex comb length illustrates the inextricable interplay between selection and variation.
abstract: In spite of the diversity of possible biological forms observed in nature, a limited range of morphospace is frequently occupied for a given trait. Several mechanisms have been proposed to explain this bias in the distribution of phenotypes including selection, drift, and developmental constraints. Despite extensive work on phenotypic bias, the underlying developmental mechanisms explaining why particular regions of morphological space remain unoccupied are poorly understood. To address this issue, we studied the sex comb, a group of modified bristles used in courtship that shows marked morphological diversity among Drosophila species. In many Drosophila species including Drosophila melanogaster, the sex comb rotates 90° to a vertical position during development. Here we analyze the effect of changing D. melanogaster sex comb length on the process of rotation. We find that artificial selection changes the number of bristles per comb without a proportional change in the space available for rotation. As a result, when increasing sex comb length, rather than displaying a similar straight vertical shape observed in other Drosophila species, long sex combs bend because rotation is blocked by a neighboring row of bristles. Our results show ways in which morphologies that would be favored by natural selection are apparently impossible to achieve developmentally. These findings highlight the potential role of development in modifying selectable variation in the evolution of Drosophila sex comb length.
authors.affiliation: Department of Cell and System Biology, University of Toronto, Toronto, ON, Canada M5S 3G5; nicolasmalagon@gmail.com singh@mcmaster.ca ellen.larsen1@gmail.com.
authors.forename: Juan N
authors.initials: JN
authors.lastname: Malagón
authors.affiliation: Department of Biology, McMaster University, Hamilton, ON, Canada L8S 4K1;
authors.forename: Abha
authors.initials: A
authors.lastname: Ahuja
authors.affiliation: Department of Cell and System Biology, University of Toronto, Toronto, ON, Canada M5S 3G5;
authors.forename: Gabilan
authors.initials: G
authors.lastname: Sivapatham
authors.affiliation: Department of Cell and System Biology, University of Toronto, Toronto, ON, Canada M5S 3G5;
authors.forename: Julian
authors.initials: J
authors.lastname: Hung
authors.affiliation: Department of Cell and System Biology, University of Toronto, Toronto, ON, Canada M5S 3G5;
authors.forename: Jiwon
authors.initials: J
authors.lastname: Lee
authors.affiliation: Department of Biochemistry and Molecular Biology, Center for Comparative Genomics and Evolutionary Bioinformatics, Dalhousie University, Halifax, NS, Canada B3H 4R2; and.
authors.forename: Sergio A
authors.initials: SA
authors.lastname: Muñoz-Gómez
authors.affiliation: Department of Entomology & Nematology, University of California, Davis, CA 95616.
authors.forename: Joel
authors.initials: J
authors.lastname: Atallah
authors.affiliation: Department of Biology, McMaster University, Hamilton, ON, Canada L8S 4K1; nicolasmalagon@gmail.com singh@mcmaster.ca ellen.larsen1@gmail.com.
authors.forename: Rama S
authors.initials: RS
authors.lastname: Singh
authors.affiliation: Department of Cell and System Biology, University of Toronto, Toronto, ON, Canada M5S 3G5; nicolasmalagon@gmail.com singh@mcmaster.ca ellen.larsen1@gmail.com.
authors.forename: Ellen
authors.initials: E
authors.lastname: Larsen
mesh_terms: D000825:Animal Structures / Q000033:anatomy & histology / Q000254:growth & development; D000818:Animals; D005075:Biological Evolution; D004330:Drosophila / Q000033:anatomy & histology* / Q000235:genetics* / Q000254:growth & development; D004331:Drosophila melanogaster / Q000033:anatomy & histology / Q000235:genetics / Q000254:growth & development; D005121:Extremities / Q000033:anatomy & histology; D008297:Male; D009024:Morphogenesis; D010641:Phenotype; D010802:Phylogeny; D012641:Selection, Genetic; D012727:Sex Characteristics; D013045:Species Specificity