Wolbachia in the Drosophila yakuba Complex: Pervasive Frequency Variation and Weak Cytoplasmic Incompatibility, but No Apparent Effect on Reproductive Isolation.
Three hybridizing species-the clade [(Drosophila yakuba, D. santomea), D. teissieri]-comprise the yakuba complex in the D. melanogaster subgroup. Their ranges overlap on Bioko and São Tomé, islands off west Africa. All three species are infected with Wolbachia-maternally inherited, endosymbiotic bacteria, best known for manipulating host reproduction to favor infected females. Previous analyses reported no cytoplasmic incompatibility (CI) in these species. However, we discovered that Wolbachia from each species cause intraspecific and interspecific CI. In D teissieri, analyses of F1and backcross genotypes show that both host genotype and Wolbachia variation modulate CI intensity. Wolbachia-infected females seem largely protected from intraspecific and interspecific CI, irrespective of Wolbachia and host genotypes. Wolbachia do not affect host mating behavior or female fecundity, within or between species. The latter suggests little apparent effect of Wolbachia on premating or gametic reproductive isolation (RI) between host species. In nature, Wolbachia frequencies varied spatially for D. yakuba in 2009, with 76% (N = 155) infected on São Tomé, and only 3% (N = 36) infected on Bioko; frequencies also varied temporally in D. yakuba and D. santomea on São Tomé between 2009 and 2015. These temporal frequency fluctuations could generate asymmetries in interspecific mating success, and contribute to postzygotic RI. However, the fluctuations in Wolbachia frequencies that we observe also suggest that asymmetries are unlikely to persist. Finally, we address theoretical questions that our empirical findings raise about Wolbachia persistence when conditions fluctuate, and about the stable coexistence of Wolbachia and host variants that modulate Wolbachia effects.
Department of Evolution and Ecology, Center for Population Biology, University of California, Davis, California 95616 brandon.cooper@mso.umt.edu.
Brandon S
0000-0002-8269-7731
BS
Cooper
Department of Evolution and Ecology, Center for Population Biology, University of California, Davis, California 95616.
Paul S
PS
Ginsberg
Department of Evolution and Ecology, Center for Population Biology, University of California, Davis, California 95616.
Michael
0000-0003-1188-9856
M
Turelli
Biology Department, University of North Carolina, Chapel Hill, North Carolina 27510.
Daniel R
0000-0002-7597-602X
DR
Matute
D000354:Africa, Western; D000818:Animals; D003433:Crosses, Genetic; D003593:Cytoplasm / Q000378:metabolism / Q000382:microbiology; D004331:Drosophila melanogaster / Q000235:genetics / Q000378:metabolism / Q000382:microbiology*; D005260:Female; D054884:Host-Pathogen Interactions; D006824:Hybridization, Genetic / Q000235:genetics*; D008297:Male; D012098:Reproduction / Q000235:genetics; D060047:Reproductive Isolation; D012726:Sexual Behavior, Animal / Q000502:physiology; D013045:Species Specificity; D020577:Wolbachia / Q000235:genetics / Q000502:physiology*
frequency variation; host-microbe interactions; hybridization; mutualism; reproductive isolation