Experimental Support That Natural Selection Has Shaped the Latitudinal Distribution of Mitochondrial Haplotypes in Australian Drosophila melanogaster

Abstract

Cellular metabolism is regulated by enzyme complexes within the mitochondrion, the function of which are sensitive to the prevailing temperature. Such thermal sensitivity, coupled with the observation that population frequencies of mitochondrial haplotypes tend to 25 associate with latitude, altitude or climatic regions across species distributions, led to the hypothesis that thermal selection has played a role in shaping standing variation in the mitochondrial DNA (mtDNA) sequence. This hypothesis, however, remains controversial, and requires evidence that the distribution of haplotypes observed in nature corresponds with the capacity of these haplotypes to confer differences in thermal tolerance. Specifically, 30 haplotypes predominating in tropical climates are predicted to encode increased tolerance to heat stress, but decreased tolerance to cold stress. We present direct evidence for these predictions, using mtDNA haplotypes sampled from the Australian distribution of Drosophila melanogaster. We show that the ability of flies to tolerate extreme thermal challenges is affected by sequence variation across mtDNA haplotypes, and that the thermal performance 35 associated with each haplotype corresponds with its latitudinal prevalence. The haplotype that predominates at low (subtropical) latitudes confers greater resilience to heat stress, but lower resilience to cold stress, than haplotypes predominating at higher (temperate) latitudes. We explore molecular mechanisms that might underlie these responses, presenting evidence that the effects are in part regulated by SNPs that do not change the protein sequence. Our 40 findings suggest that standing variation in the mitochondrial genome can be shaped by thermal selection, and could therefore contribute to evolutionary adaptation under climatic stress.

Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation*

“…; Camus et al. ), while also raising questions about the scope of “faster‐X effects” in adaptive evolution (i.e., the extent to which X‐linked genes diverge more rapidly than autosomal genes during adaptation; Presgraves, , ; Meisel and Connallon ; Lasne et al. ; Charlesworth et al.…”

“…For example, Camus et al. () recently linked geographic variation in mitochondrial haplogroups to clinal divergence in thermal performance traits between tropical and temperate Australian populations of D. melanogaster . Our study suggests that the mitochondrial genome's contribution to local adaptation may not be limited to thermotolerance traits, but rather extends to starvation resistance, desiccation resistance, and potentially other physiological performance traits.…”

“…Likewise, although mitochondrial genomes are known to contribute substantially to local adaptation in some instances (e.g., Camus et al. ), the overall contribution of mitochondrial genes to local adaptation remains an open question.…”

Mitochondrial variation in small brown planthoppers linked to multiple traits and probably reflecting a complex evolutionary trajectory

“…Since then, evidence in support of mitochondrial climatic adaptation has accumulated, although most is indirect from statistical tests of neutral models of molecular evolution involving dN/dS based inference, or from correlation analyses of frequencies of mtDNA variation and environmental factors (Foote et al, ; Morales et al, ; Silva et al, ). In contrast, empirical data to test the phenotypic impact of mtDNA variants on adaptive evolution are still scarce, although studies have found experimental support for mitochondrial climatic adaptation in Drosophila simulans (Ballard, Melvin, Katewa, & Maas, ; Pichaud, Ballard, Tanguay, & Blier, ), D. melanogaster (Camus, Wolff, Sgro, & Dowling, ) , and Fundulus heteroclitus (Dhillon & Schulte, ).…”

Digest: All genomes are not equal: How variation in autosomal, sex chromosome, and mitochondrial genomes contributes to the process of local adaptation*

“…Although recent work has made predictions about the importance of different genomes for adaptation, namely, the mitochondrial genome (e.g., Camus et al. ), there is little experimental evidence available for the relative contributions of autosomal chromosomes, sex chromosomes, and mitochondrial genomes to adaptive trait divergence and local adaptation.…”