A Major Locus Controls a Genital Shape Difference Involved in Reproductive Isolation Between Drosophila yakuba and Drosophila santomea.
Rapid evolution of genitalia shape, a widespread phenomenon in animals with internal fertilization, offers the opportunity to dissect the genetic architecture of morphological evolution linked to sexual selection and speciation. Most quantitative trait loci (QTL) mapping studies of genitalia divergence have focused on Drosophila melanogaster and its three most closely related species, D. simulans, D. mauritiana, and D. sechellia, and have suggested that the genetic basis of genitalia evolution involves many loci. We report the first genetic study of male genitalia evolution between D. yakuba and D. santomea, two species of the D. melanogaster species subgroup. We focus on male ventral branches, which harm females during interspecific copulation. Using landmark-based geometric morphometrics, we characterized shape variation in parental species, F1 hybrids, and backcross progeny and show that the main axis of shape variation within the backcross population matches the interspecific variation between parental species. For genotyping, we developed a new molecular method to perform multiplexed shotgun genotyping (MSG), which allowed us to prepare genomic DNA libraries from 365 backcross individuals in a few days using little DNA. We detected only three QTL, one of which spans 2.7 Mb and exhibits a highly significant effect on shape variation that can be linked to the harmfulness of the ventral branches. We conclude that the genetic architecture of genitalia morphology divergence may not always be as complex as suggested by previous studies.
UMR7592, Institut Jacques Monod, CNRS, Univ Paris Diderot, Sorbonne Paris Cité, 75013 Paris, France alexandre.peluffo@ijm.fr virginie.orgogozo@normalesup.org.
Alexandre E
http://orcid.org/0000-0001-7216-4205
AE
Peluffo
UMR7592, Institut Jacques Monod, CNRS, Univ Paris Diderot, Sorbonne Paris Cité, 75013 Paris, France.
Isabelle
I
Nuez
UMR MNHN/MNHN/UPMC/EPHE 7205, Institut de Systématique, Evolution et Biodiversité, Muséum National d'Histoire Naturelle, 75005 Paris, France.
Vincent
V
Debat
UMR7592, Institut Jacques Monod, CNRS, Univ Paris Diderot, Sorbonne Paris Cité, 75013 Paris, France.
Rosina
R
Savisaar
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia 20147.
David L
DL
Stern
UMR7592, Institut Jacques Monod, CNRS, Univ Paris Diderot, Sorbonne Paris Cité, 75013 Paris, France alexandre.peluffo@ijm.fr virginie.orgogozo@normalesup.org.
Virginie
V
Orgogozo
D000818:Animals; D005075:Biological Evolution; D002874:Chromosome Mapping; D059006:Chromosomes, Insect; D003433:Crosses, Genetic; D004330:Drosophila / Q000033:anatomy & histology* / Q000196:embryology / Q000235:genetics*; D005260:Female; D056726:Genetic Association Studies; D005819:Genetic Markers; D005835:Genitalia / Q000033:anatomy & histology* / Q000196:embryology; D005838:Genotype; D008297:Male; D008957:Models, Genetic; D010641:Phenotype; D040641:Quantitative Trait Loci; D060047:Reproductive Isolation; D013045:Species Specificity
D005819:Genetic Markers
Drosophila; QTL; genitalia; lock-and-key; shape