Relaxed selection on male mitochondrial genes in DUI bivalves eases the need for mitonuclear coevolution

Abstract

Almost all eukaryotes rely on mitochondria and mitochondrial (mt)-encoded genes to generate cellular energy via oxidative phosphorylation (OXPHOS) (Karnkowska et al., 2016;Roger et al., 2017). Mt-encoded genes must coordinate with nuclear-encoded mt genes (i.e. N-mt genes) for OXPHOS. Coevolution and coadaptation between mt and N-mt genes are therefore essential and likely a ubiquitous feature of eukaryotes (Havird et al., 2019b;

Lack of transcriptional coordination between mitochondrial and nuclear oxidative phosphorylation genes in the presence of two divergent mitochondrial genomes

“…It is worth mentioning that positive selection on M-type has also been reported in other DUI species ( Ort & Pogson, 2007 ; Śmietanka et al, 2009 ), and that selection on M-type inferred by population genetic tests (e.g., McDonald-Kreitman test) and phylogeny-based method (e.g., dN/dS) have been inconsistent in many cases ( Ort & Pogson, 2007 ; Śmietanka et al, 2009 ; Zbawicka et al, 2010 ). In R. philippinarum , phylogenetic analysis indicated relaxed selection on most M-type OXPHOS genes ( Maeda et al, 2021 ), whereas population tests in this study showed a signal of positive selection or balancing selection. Although demographic events or bottleneck differences may influence population-based methods, several genes such as COX3 and NAD3 showed the same signal between the two methods.…”

“…It is worth mentioning that Maeda et al ( 2021 ) found two divergent SDHC sequences in their study and one of them ( SDHC -2) showed a gonad-specific transcription (Supplementary Figure S3B). Around half of the nuclear genes co-transcribed with nuOXPHOS were correlated only with the SDHC -2, which might explain the presence of enriched GO terms involved in the cell cycle (Supplementary Table S6).…”

“…Adductor muscle, mantle, and gonad from 15 males and 15 females (with the exception of a missing female mantle; 89 samples in total) were sequenced using Illumina HiSeq 2500 with insert size of 500 bp to generate 150 bp paired-end reads. Detailed information about RNA extraction, library preparation, sequencing and de novo transcriptome assembly can be found in Maeda et al ( 2021 ). The de novo reference transcriptome assembly for R. philippinarum is available on the Transcriptome Shotgun Assembly Sequence Database (TSA) of NCBI (accession No.…”

“…Nuclear OXPHOS transcripts were retrieved from Maeda et al ( 2021 ) (BioProject PRJNA672267). To get coding sequences from nuOXPHOS transcripts, we ran TransDecoder (https://github.com/TransDecoder/TransDecoder/wiki) using homology searches against nr and Pfam databases with the minimum length of the open reading frame of 150 bp and only the longest ORF for each OXPHOS gene was kept.…”

“…However, other studies have hypothesized that M-type may have undergone adaptive evolution optimizing sperm/male gonad functions ( Bettinazzi et al, 2019 , 2020 ; Burt & Trivers, 2006 ; Ghiselli et al, 2013 , 2021a , 2021b ; Iannello et al, 2019 ; Skibinski et al, 1994 , 2017 ). Therefore, studying selection on different OXPHOS genes would be critical to understanding how two divergent mt genomes evolve with the same nuOXPHOS genes ( Iannello et al, 2019 ; Maeda et al, 2021 ; Piccinini et al, 2021 ).…”