Divergent mitochondrial and nuclear OXPHOS genes are candidates for genetic incompatibilities in Ficedula Flycatchers

Abstract

Hybrid dysfunction is an important source of reproductive isolation between emerging species. Bateson-Dobzhansky-Muller incompatibilities are theoretically well-recognized as the underlying cause of low hybrid dysfunction. However, especially in wild populations, little empirical evidence exists for which genes are involved in such incompatibilities. The relative role of ecological divergence in causing the build-up of genetic incompatibilities in relation to other processes such as genomic conflict therefore remains largely unknown. Genes involved in energy metabolism are potential candidates for genetic incompatibilities, since energy metabolism depends on co-expression of mitochondrial DNA (mtDNA) and nuclear DNA (nDNA) leading to mitonuclear coadaptation. When mitochondrial and nuclear genes lacking a co-evolutionary history appear together in hybrids, incompatibilities could arise. Ficedula flycatcher F1 hybrids have a higher resting metabolic rate (RMR) compared to the parental species, which could be a sign of genetic incompatibilities between energy metabolism genes that diverged in response to environmental differences while the species were in allopatry. Based on sequences of 15 mitochondrial genes of 264 individuals, we show that the two species have divergent mtDNA caused by the build-up of mainly synonymous mutations and a few non-synonymous mutations. Pied flycatcher mitogenomes show evidence of non-neutrality, indicating a selective sweep or population expansion. There is little variation in the nuclear OXPHOS-related proteins and no significant deviation from neutrality, however, specific codon identified sites might be under positive selection in both mitochondrial and nuclear genes encoding OXPHOS proteins for complex I and III. Taken together, these diverged mitonuclear genes therefore constitute possible candidates underlying, at least part of the genetic incompatibilities that cause hybrid dysfunction in crosses between collared and pied flycatchers.