Abstract
Mitochondrial DNA (mtDNA) consists of few but vital maternally inherited genes that interact closely with nuclear genes to produce cellular energy. How important mtDNA polymorphism is for adaptation is still unclear. The assumption in population genetic studies is often that segregating mtDNA variation is selectively neutral. This contrasts with empirical observations of mtDNA haplotypes affecting fitness‐related traits and thermal sensitivity, and latitudinal clines in mtDNA haplotype frequencies. Here, we experimentally test whether ambient temperature affects selection on mtDNA variation, and whether such thermal effects are influenced by intergenomic epistasis due to interactions between mitochondrial and nuclear genes, using replicated experimental evolution in Callosobruchus maculatus seed beetle populations seeded with a mixture of different mtDNA haplotypes. We also test for sex‐specific consequences of mtDNA evolution on reproductive success, given that mtDNA mutations can have sexually antagonistic fitness effects. Our results demonstrate natural selection on mtDNA haplotypes, with some support for thermal environment influencing mtDNA evolution through mitonuclear epistasis. The changes in male and female reproductive fitness were both aligned with changes in mtDNA haplotype frequencies, suggesting that natural selection on mtDNA is sexually concordant in stressful thermal environments. We discuss the implications of our findings for the evolution of mtDNA.
Highlights
Mitochondria have a central role in cellular energy metabolism regulated by enzyme complexes encoded by both mitochondrial and nuclear genes (Blier, Dufresne, & Burton, 2001; Rand, Haney, & Fry, 2004)
Our results demonstrate that mitochondrial DNA (mtDNA) haplotype frequency dynamics are nonrandom and that they are contingent upon thermal conditions, providing experimental evidence against the widely held assumption of neutrality of segregating mitochondrial genetic variation
We show that mtDNA haplotype frequency changes during experimental evolution are associated with changes in lifetime reproductive success across lines
Summary
Mitochondria have a central role in cellular energy metabolism regulated by enzyme complexes encoded by both mitochondrial and nuclear genes (Blier, Dufresne, & Burton, 2001; Rand, Haney, & Fry, 2004). Mitochondrial genes have traditionally been thought to evolve under strong purifying selection, due to their vital role in cellular respiration, with only selectively neutral mitochondrial mutations segregating as common alleles within and among populations (Ballard & Kreitman, 1994; Rand, 2001) These views have been questioned by several lines of evidence suggesting that polymorphisms in mitochondrial DNA (mtDNA) show signatures of recurrent adaptive evolution (Bazin, Glemin, & Galtier, 2006; Galtier, Nabholz, Glemin, & Hurst, 2009; James, Piganeau, & Eyre-Walker, 2016) and contribute to variation in fitness-related traits (Burton, Pereira, & Barreto, 2013; Dobler, Rogell, Budar, & Dowling, 2014; Dordevic et al, 2017; Dowling, Friberg, & Lindell, 2008; Immonen, Collet, Goenaga, & Arnqvist, 2016; Immonen, Ronn, Watson, Berger, & Arnqvist, 2016; Rand, Clark, & Kann, 2001; Wolff et al, 2016). We predicted that such non-neutral effects may influence mtDNA evolution under stressful thermal conditions, with putatively sex-specific fitness consequences
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