Intergenomic interactions between mitochondrial and Y-linked genes shape male mating patterns and fertility in Drosophila melanogaster

Evolution. 2015 Nov;69(11):2876-90. doi: 10.1111/evo.12788. Epub 2015 Oct 16.

Abstract

Under maternal inheritance, mitochondrial genomes are prone to accumulate mutations that exhibit male-biased effects. Such mutations should, however, place selection on the nuclear genome for modifier adaptations that mitigate mitochondrial-incurred male harm. One gene region that might harbor such modifiers is the Y-chromosome, given the abundance of Y-linked variation for male fertility, and because Y-linked modifiers would not exert antagonistic effects in females because they would be found only in males. Recent studies in Drosophila revealed a set of nuclear genes whose expression is sensitive to allelic variation among mtDNA- and Y-haplotypes, suggesting these genes might be entwined in evolutionary conflict between mtDNA and Y. Here, we test whether genetic variation across mtDNA and Y haplotypes, sourced from three disjunct populations, interacts to affect male mating patterns and fertility across 10 days of early life in D. melanogaster. We also investigate whether coevolved mito-Y combinations outperform their evolutionarily novel counterparts, as predicted if the interacting Y-linked variance is comprised of modifier adaptations. Although we found no evidence that coevolved mito-Y combinations outperformed their novel counterparts, interactions between mtDNA and Y-chromosomes affected male mating patterns. These interactions were dependent on male age; thus male reproductive success was shaped by G × G × E interactions.

Keywords: Adaptation; genomic conflict; male fertility; mitonuclear; mtDNA; sexual conflict.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • Biological Evolution*
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / physiology
  • Female
  • Fertility / genetics*
  • Genes, Insect
  • Genes, Mitochondrial*
  • Genes, Y-Linked*
  • Genetic Variation
  • Haplotypes
  • Male
  • Reproduction / genetics

Associated data

  • Dryad/10.5061/dryad.GH350