New View on the Organization and Evolution of Palaeognathae Mitogenomes Poses The Question on the Ancestral Gene Rearrangement in Aves

Abstract

BackgroundBird mitogenomes differ from other vertebrates in gene rearrangement. The most common avian gene order, first identified in Gallus gallus, is considered ancestral for all Aves. However, other rearrangements including a duplicated control region and neighboring genes have been reported in many representatives of avian orders. The repeated regions can be easily omitted due to inappropriate DNA amplification or genome sequencing, and may thus be readily overlooked. This raises a question about the actual prevalence of mitogenomic duplications and the validity of the current view on the avian mitogenome evolution. In this context, Palaeognathae is especially interesting because is sister to all other living birds (Neognathae). So far, a unique duplicated region has been found in one palaeognath mitogenome, that of Eudromia elegans. ResultsTherefore, we applied an appropriate PCR strategy to look for omitted duplications in other palaeognaths. The analyses revealed the duplicated control regions with adjacent genes in Crypturellus, Rhea and Struthio as well as ND6 pseudogene in three moa. The copies are very similar and were subjected to concerted evolution. Mapping the presence and absence of duplication onto the Palaeognathae phylogeny indicates that the duplication was an ancestral state for this avian group. This feature was inherited by early diverged lineages and lost two times in others. Comparison of incongruent phylogenetic trees based on mitochondrial and nuclear sequences showed that two variants of mitogenomes could exist in the evolution of palaeognaths. Included data for other avian mitogenomes revealed that the last common ancestor of all birds and early diverging lineages of Neoaves may also possess the mitogenomic duplication.ConclusionsThe duplicated control regions with adjacent genes are more common in avian mitochondrial genomes than it was previously thought. These two regions could increase effectiveness of replication and transcription as well as the number of replicating mitogenomes per organelle. In consequence, energy production by mitochondria may be also more efficient. However, further physiological and molecular analyses are necessary to assesses the potential selective advantages of the mitogenome duplications.

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“…Our result supports the hypothesis that nad6 duplication could be widespread in Procellariiformes ( Torres et al 2019 ), and, like cob , could have undergone various events of deletion or addition during the diversification of the order. Nevertheless, because some of the reported duplications could be artificial ( Urantówka et al 2020 ; Formenti et al 2021 ), to fully identify the true number of gene duplications/deletions will require additional and specific experimental analyses.…”