Mitochondrial-Y chromosome epistasis inDrosophila melanogaster

Abstract

The coordination between mitochondrial and nuclear genes is crucial to eukaryotic organisms. Predicting the nature of these epistatic interactions can be difficult because of the transmission asymmetry of the genes involved. While autosomes and X-linked genes are transmitted through both sexes, genes on the Y chromosome and in the mitochondrial genome are uniparentally transmitted through males and females, respectively. Here, we generate 36 otherwise isogenic Drosophila melanogaster strains differing only in the geographical origin of their mitochondrial genome and Y chromosome, to experimentally examine the effects of the uniparentally inherited parts of the genome, as well as their interaction, in males. We assay longevity and gene expression through RNA-sequencing. We detect an important role for both mitochondrial and Y-linked genes, as well as extensive mitochondrial-Y chromosome epistasis. In particular, genes involved in male reproduction appear to be especially sensitive to such interactions, and variation on the Y chromosome is associated with differences in longevity. Despite these interactions, we find no evidence that the mitochondrial genome and Y chromosome are co-adapted within a geographical region. Overall, our study demonstrates a key role for the uniparentally inherited parts of the genome for male biology, but also that mito-nuclear interactions are complex and not easily predicted from simple transmission asymmetries.

Adaptive co‐evolution of mitochondria and the Y‐chromosome: A resolution to conflict between evolutionary opponents

“…Y chromosome variation (Branco et al, 2013) disproportionately affects mitochondriarelated genes and genes whose expression is affected by mitochondrial haplotype are affected as well by Y-chromosome variation (Guo, 2015;Rogell et al, 2014). Experimental studies in D. melanogaster have revealed Y-mt epistatic interactions for male reproduction, including effects on male fertility and mating success (Ågren et al, 2019b;Yee et al, 2015). Although many of the data cited here are from experiments involving between-population crosses, we note that many genetic phenomena were discovered and are studied in inter-population crosses, including cytoplasmic inheritance, the ubiquitous arthropod microbe Wolbachia, meiotic Y-mt combinations have the highest male fertility is present in some studies but not in all (Ågren et al, 2019b;Yee et al, 2013).…”

“…Experimental studies in D . melanogaster have revealed Y‐mt epistatic interactions for male reproduction, including effects on male fertility and mating success (Ågren et al, 2019b; Yee et al, 2015). Although many of the data cited here are from experiments involving between‐population crosses, we note that many genetic phenomena were discovered and are studied in inter‐population crosses, including cytoplasmic inheritance, the ubiquitous arthropod microbe Wolbachia, meiotic drive and its suppressors, p‐elements and their suppressors, and Dobzhansky‐Muller incompatibilities.…”

“…For rapidly evolving phenomena within populations, polymorphisms are likely to be transient; making it is easier to discover phenomena in interspecific crosses between populations, where the same processes have arrived at different equilibria. The evidence for adaptive epistasis in which native Y‐mt combinations have the highest male fertility is present in some studies but not in all (Ågren et al, 2019b; Yee et al, 2013). Although, in such experiments, a finding of highest fitness on the home (or non‐novel) genetic background is typically interpreted evidence of coadaptation (see e.g., Ågren et al, 2019b for more details), some authors have hypothesized that their findings were owing to repeated cycles of mitochondrial harm to male fertility followed by autosomal restoration.…”

“…The evidence for adaptive epistasis in which native Y‐mt combinations have the highest male fertility is present in some studies but not in all (Ågren et al, 2019b; Yee et al, 2013). Although, in such experiments, a finding of highest fitness on the home (or non‐novel) genetic background is typically interpreted evidence of coadaptation (see e.g., Ågren et al, 2019b for more details), some authors have hypothesized that their findings were owing to repeated cycles of mitochondrial harm to male fertility followed by autosomal restoration. This interpretation is the only one possible when the conclusions of established theory rule out direct coadaptation between a Y‐linked gene and a mitochondrial gene.…”

“…These single gene cytoplasmic models did not examine Y‐mitochondrial gene interactions or any kind of nuclear‐mitochondrial epistasis for fitness. Empirically, however, studies by Dean et al (2015), Yee et al (2015), and Ågren et al (2019b) in Drosophila melanogaster discovered abundant mitochondrial‐Y chromosome epistasis. The findings of Ågren et al (2019b, p. 1) are that, “In particular, genes involved in male reproduction appear to be especially sensitive to such interactions.” In this article, we examine theoretically the potential for coevolution between Y‐linked and mitochondrial genes.…”