EUROPEAN JOURNAL OF ENTOMOLOGY

Eur. J. Entomol. 116: 492-503, 2019 | DOI: 10.14411/eje.2019.051

Local adaptation at fine spatial scale through chromosomal inversions and mito-nuclear epistasis: Findings in Drosophila subobscura (Diptera: Drosophilidae)Original article

Marija SAVIĆ VESELINOVIĆ¹, Zorana KURBALIJA NOVIČIĆ^3,4, Bojan KENIG⁵, Mihailo JELIĆ¹, Aleksandra PATENKOVIĆ², Marija TANASKOVIĆ², Cino PERTOLDI^6,7, Marina STAMENKOVIĆ-RADAK^1,2, Marko ANDJELKOVIĆ⁸

¹ Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia; e-mails: marijas@bio.bg.ac.rs, mihailoj@bio.bg.ac.rs, marina@bio.bg.ac.rs

² Institute for Biological Research “Siniša Stanković” - National Institute of Republic of Serbia, University of Belgrade, Despot Stefan Blvd. 142, 11000 Belgrade, Serbia; e-mails: aleksandra@ibiss.bg.ac.rs, marija.tanaskovic@ibiss.bg.ac.rs

³ Animal Ecology, Department of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden; e-mail: zorana.novicic@neuro.uu.se

⁴ Department of Neuroscience, Psychiatry, Uppsala University, SE-751 24 Uppsala, Sweden

⁵ Center for the Promotion of Science, Belgrade, Serbia; e-mail: bkenig@cpn.rs

⁶ Department 18 / Section of Environmental Engineering, Aalborg University, Aalborg, Denmark; e-mail: cp@bio.aau.dk

⁷ Aalborg Zoo, Aalborg, Denmark

⁸ Serbian Academy of Sciences and Arts, Knez Mihailova 35, 11000 Belgrade, Serbia; e-mail: marko.andjelkovic@sanu.ac.rs

To explore local adaptation in wild populations at a fine spatial scale we characterized the genetic variability of eight closely located populations of Drosophila subobscura and its associations with microhabitat environmental conditions. Three different genetic markers were assessed: chromosomal inversions, a SNP of mitochondrial ND5 gene and nuclear microsatellites. Population genetic analyses of chromosomal variability revealed significant genetic differentiation between these populations. Gene arrangement frequencies on the E chromosome contributed most to these differences. We also investigated role of mito-nuclear epistasis in mitochondrial genome differentiation and revealed weak linkage disequilibrium (LD) exclusively between O₃₊₄ inversion arrangement and mitochondrial DNA haplotype I in two populations. In addition, the trend in the LD between O_ST chromosomal arrangement and haplotype II was general in the total sample. Microsatellite analysis revealed an absence of stochastic processes, like census reduction, upon population differentiation. Only a small amount of the genetic variation is related to geographic distance, while most (97%) is attributable to other factors and in some degree to microhabitat variables (temperature, humidity). The analysis of these factors revealed they effect inversion arrangement frequencies, especially E₁₊₂₊₉, E_ST and O_ST. Even though this model organism is known for its high mobility and mostly large effective population size, the results presented here reveal that local adaptations can occur even at a small spatial scale. We propose that locally adapted alleles within chromosomal inversions, as well as joint selective pressures acting on mitochondrial and nuclear genomes, are responsible for the observed adaptation to microhabitat conditions.

Keywords: Diptera, Drosophilidae, Drosophila subobscura, genetic differentiation, high dispersion, chromosomal inversion, ND5, microsatellites, local adaptation

Received: October 4, 2019; Accepted: December 3, 2019; Published online: December 30, 2019  Show citation