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Mitochondrial genome evolution in Annelida: A systematic study on conservative and variable gene orders and the factors influencing its evolution

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Apr 28, 2023 version files 31.75 MB

Abstract

The mitochondrial genomes of Bilateria are relatively conserved in their protein-coding, rRNA and tRNA gene complement, but the order of these genes can range from very conserved to very variable depending on the taxon. The supposedly conserved gene order of Annelida has been used to support the placement of some taxa within Annelida. Recently, authors have cast doubts on the conserved nature of the annelid gene order. Various factors may influence gene-order variability including, among others, increased substitution rates, base composition differences, structure of non-coding regions, parasitism, living in extreme habitats, short generation times and biomineralization. However, these analyses were neither done systematically, nor based on well-established reference trees. Several focused on only a few of these factors and biological factors were usually explored ad-hoc without rigorous testing or correlation analyses. Herein, we investigated the variability and evolution of the annelid gene order and the factors that potentially influenced its evolution, using a comprehensive and systematic approach. The analyses were based on 170 genomes, including 33 previously unrepresented species. Our analyses included 706 different molecular properties, 20 life-history and ecological traits and a reference tree corresponding to recent improvements concerning the annelid tree. The results showed that the gene order with and without tRNAs is generally conserved. However, individual taxa exhibit higher degrees of variability. None of the analyzed life-history and ecological traits explained the observed variability across mitochondrial gene orders. In contrast, the combination and interaction of the best predicting factors for substitution rate and base composition explained up to 30% of the observed variability. Accordingly, correlation analyses of different molecular properties of the mitochondrial genomes showed an intricate network of direct and indirect correlations between the different molecular factors. Hence, gene order evolution seems to be driven by molecular evolutionary aspects rather than by life history or ecology. On the other hand, gene order variability does not predict difficulty in placing certain taxa within molecular phylogenetic studies. We also discuss the molecular properties of annelid mitochondrial genomes considering canonical views on gene evolution and potential reasons why they do not always fit to the observed patterns without nuisance.