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

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.

两侧对称动物（Bilateria）的线粒体基因组（mitochondrial genomes）在其编码蛋白、核糖体RNA（rRNA）和转运RNA（tRNA）的基因组成上相对保守，但这些基因的排列顺序却因类群不同，从高度保守到高度可变不等。环节动物门（Annelida）的基因排列顺序被认为具有保守性，这一特征曾被用于支持部分类群归入环节动物门。近年来，有学者对环节动物基因排列顺序的保守性提出了质疑。诸多因素均可影响基因排列的变异性，具体包括替换率升高、碱基组成差异、非编码区结构、寄生生活、极端生境栖息、短世代时间以及生物矿化作用等。不过，此前的相关分析既未采用系统化的研究框架，也未基于经过验证的完善参考系统发育树。部分研究仅聚焦于其中少数几种因素，且针对生物学相关因素的探讨通常仅为临时性的个案分析，未经过严格检验或相关性分析。本研究采用全面且系统化的方法，探究了环节动物线粒体基因排列的变异性与进化过程，以及潜在影响其进化的各类因素。本次分析基于170个线粒体基因组，其中包含33个此前未被收录的物种，涵盖了706项不同的分子特征、20项生活史与生态性状，以及基于近期环节动物系统发育研究进展构建的参考系统发育树。研究结果显示，无论是否包含tRNA基因，线粒体基因的整体排列大多呈现保守状态，但个别类群的基因排列变异性较高。本研究所分析的所有生活史与生态性状，均无法解释观测到的线粒体基因排列变异情况。与之相反，替换率与碱基组成的最优预测因子的组合及其交互作用，可解释高达30%的观测变异。对线粒体基因组不同分子特征的相关性分析显示，各类分子因素之间存在复杂的直接与间接关联网络。由此可见，基因排列的进化似乎主要由分子进化层面的因素驱动，而非生活史或生态特征。此外，基因排列的变异性无法预测某些类群在分子系统发育研究中的分类定位难度。本研究还结合基因进化的经典理论，探讨了环节动物线粒体基因组的分子特征，以及在排除无关干扰因素的前提下，为何这些特征并不总是与观测到的进化模式相符的潜在原因。