Potentially adaptive mitochondrial haplotypes as a tool to identify divergent nuclear loci

Abstract

Summary Genetic tools are commonly used for conservation and management of at‐risk species. Individuals are often sampled from mixtures that are composed of many populations, which creates a need to assign individuals to their source. This can be problematic when the genetic divergence among source populations is weak but can be improved using adaptive genetic loci, which should show stronger levels of divergence. We previously reported a signature of positive selection in the mitochondrial‐encoded ND5 subunit of complex I in diverse taxa. The respiratory machinery of the mitochondria in salmonids is composed of more than 80 nuclear genes and there is substantial interaction between nuclear and mitochondrial expressed gene products. Recent studies report adaptive variation in mitochondrial function as well as co‐evolution between mitochondrial and nuclear genomes. We used potentially adaptive ND5‐based mitochondrial haplotypes to identify nuclear loci that would display increased levels of genetic divergence compared to neutral nuclear loci in chum salmon (Oncorhynchus keta). Populations in a geographic area the size of France have previously demonstrated weak genetic divergence even after substantial discovery efforts by multiple laboratories for allozymes, microsatellites and SNPs over the last two decades. We used RAD‐based next‐generation sequencing and identified a nuclear‐encoded subunit of mitochondrial complex I that was a significant FST outlier and 14 other divergent nuclear markers that improve genetic assignment of individuals to their population of origin relative to assignments based on neutral markers alone. This work demonstrates how a known adaptive marker can be leveraged to increase the probability of identifying divergent markers for applied genetics tools that may be biologically linked to it.

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

“…Although mechanisms underlying interactions are unclear, our protein modelling predicts that the amino acid changes in ND2 and ND5 may interact with the residues of nuclear coded subunits NDUFA10 and CYC1 respectively, which might be associated with reduced complex I assembly and activity, and be responsible for the mitonuclear interactions in SBPH. In support of this result, ND2/ND10 subunits were found to be part of mitonuclear co‐evolution in salmonids (Garvin et al, ).…”

New insights into and limitations of the molecular phylogeny in the taxon‐rich land snail genusMontenegrina(Mollusca: Gastropoda: Clausiliidae)

“…The fact that, within Montenegrina , several amino acid changes in the COI protein were deduced from the DNA data set is in contrast with a single variable site found in the genus Alopia (Fehér et al., 2013). Nonetheless, it remains speculative whether these replacements are conserved in a clade‐specific manner due to episodes of positive selection, as has been shown for several animals and various mt genes (Garvin, Bielawski, Sazanov, & Gharrett, 2015; Garvin et al., 2017; Slimen, Allio, & Jacques, 2016).…”

Assessing the fitness consequences of mitonuclear interactions in natural populations

“…Such approaches have inferred climate‐driven positive selection in mitochondrial‐encoded Complex I components in a range of animal taxa (Finch et al ., ; Garvin et al ., ; Caballero et al ., ). Structural mapping has also recently provided evidence of epistatic interactions between mitochondrial‐encoded and nuclear‐encoded Complex I variants potentially under climate‐driven selection (Garvin et al ., ; Morales et al ., ). As we have noted, mitonuclear incompatibilities need not involve direct interactions within multi‐subunit complexes (Innocenti et al ., ; Baris et al ., ).…”