Experimental evidence that thermal selection shapes mitochondrial genome evolution

Abstract

Mitochondria are essential organelles, found within eukaryotic cells, which contain their own DNA. Mitochondrial DNA (mtDNA) has traditionally been used in population genetic and biogeographic studies as a maternally-inherited and evolutionary-neutral genetic marker. However, it is now clear that polymorphisms within the mtDNA sequence are routinely non-neutral, and furthermore several studies have suggested that such mtDNA polymorphisms are also sensitive to thermal selection. These observations led to the formulation of the “mitochondrial climatic adaptation” hypothesis, for which all published evidence to date is correlational. Here, we use laboratory-based experimental evolution in the fruit fly, Drosophila melanogaster, to test whether thermal selection can shift population frequencies of two mtDNA haplogroups whose natural frequencies exhibit clinal associations with latitude along the Australian east-coast. We present experimental evidence that the thermal regime in which the laboratory populations were maintained drove changes in haplogroup frequencies across generations. Our results strengthen the emerging view that intra-specific mtDNA variants are sensitive to selection, and suggest spatial distributions of mtDNA variants in natural populations of metazoans might reflect adaptation to climatic environments rather than within-population coalescence and diffusion of selectively-neutral haplotypes across populations.

The association between mitochondrial genetic variation and reduced colony fitness in an invasive wasp

“…Through whole mitochondrial genome sequencing, we found variation in the number of tandem repeats in the control region in two samples, although this variation on its own did not seem to be strongly associated with haplotype fitness. However, our overall findings add to evidence that synonymous substitutions or changes in noncoding regions could affect mitochondrial function (Camus et al, ; Lajbner et al, ).…”

Size does matter: Parallel evolution of adaptive thermal tolerance and body size facilitates adaptation to climate change in domestic cattle

“…Furthermore, body temperature variation is associated with reduced fitness, with more extreme daily fluctuations correlated with reduced reproduction in wild mammal populations (Maloney, Marsh, McLeod, & Fuller, ). Cells recognize environmental fluctuations through sophisticated signaling pathways and hence stress directly affects the cellular integrity, function, and morphology (Rabouille & Alberti, ) and shapes mitochondrial genome evolution (Lajbner et al, ). The maintenance of homeothermy during heat stress in SCB was achieved primarily by heterothermy.…”

“…The phylogeny revealed that Vechur and Wayanad clustered in the Indicus 1 haplotype (I1), while Kasargode clustered in the Indicus 2 (I2) haplotype, showing a convergent evolution of dwarf size in response to high heat and humidity in cattle breeds in different regions (Taye et al, ). The mitochondrial genome of dwarf cattle might have evolved through selection under heat stress (Lajbner et al, ). In domestic cattle, dwarfing and tolerance is evolutionarily defined by functional traits developed through maternal founder effect and adaptation to warm environments (Lenstra et al, ).…”

“…Thus, by simultaneously measuring both physiological and molecular responses, it is possible to assess differential tolerance among dissimilar genetic groups of animals (Albon et al, ; Alfonzo et al, ; Mitchell et al, ). Additionally, mitogenome analysis can map out the observed differential adaptive trait variations at physiological and molecular levels to the phylogeny of different genetic groups (Lajbner, Pnini, Camus, Miller, & Dowling, ).…”

“…Specifically, we evaluated the effects of acute heat stress, and rates of climatic‐niche evolution of functional traits, in a morphologically distinct population of domestic cattle. Next, we determined whether the variation in traits changed systematically across genetic groups representing different molecular mitochondrial phylogenetic scales by mapping evolutionary processes on to the trait diversity (Lajbner et al, ). Thus, we explored the potential for integrating physiological responses with molecular phylogeny to appreciate the physiological and evolutionary costs of body size changes.…”