Data for dating in the dark: Elevated substitution rates in cave cockroaches (Blattodea: Nocticolidae) have negative impacts on molecular date estimates

Rates of nucleotide substitution vary substantially across the Tree of Life, with potentially confounding effects on phylogenetic and evolutionary analyses. A large acceleration in mitochondrial substitution rate occurs in the cockroach family Nocticolidae, which predominantly inhabit subterranean environments. To evaluate the impacts of this among-lineage rate heterogeneity on estimates of phylogenetic relationships and evolutionary timescales, we analysed nuclear ultraconserved elements (UCEs) and mitochondrial genomes from nocticolids and other cockroaches. Substitution rates were substantially elevated in nocticolid lineages compared with other cockroaches, especially in mitochondrial protein-coding genes. This disparity in evolutionary rates is likely to have led to different evolutionary relationships being supported by mitochondrial genomes and UCE loci. Furthermore, analyses using relaxed-clock models inferred much deeper divergence times compared with a flexible local clock. Our phylogenetic analysis of UCEs, which is the first genome-scale study to include all nine major cockroach families, unites Corydiidae and Nocticolidae and places Anaplectidae as the sister lineage to the rest of Blattoidea. We uncover an extraordinary level of genetic divergence in Nocticolidae, including two highly distinct clades that separated ~115 million years ago despite both containing representatives of the genus Nocticola. The results of our study highlight the potential impacts of high among-lineage rate variation on estimates of phylogenetic relationships and evolutionary timescales.

核苷酸替换速率在生命之树（Tree of Life）各分支间存在显著差异，这可能对系统发育与进化分析造成混淆性影响。诺氏蠊科（Nocticolidae）的线粒体替换速率发生大幅提升，该类群主要栖息于地下环境。为评估这种谱系间速率异质性对系统发育关系与进化时间尺度估算的影响，本研究分析了诺氏蠊科（Nocticolidae）及其他蜚蠊的核基因组超保守元件（ultraconserved elements, UCEs）与线粒体基因组。相较于其他蜚蠊，诺氏蠊谱系的替换速率显著升高，尤其是在线粒体蛋白编码基因中。这种进化速率的差异可能导致线粒体基因组与UCE位点所支持的进化关系出现分歧。此外，相较于灵活局部钟模型，采用宽松分子钟模型（relaxed-clock models）的分析推断出的分化时间要古老得多。本研究针对UCEs的系统发育分析是首个涵盖全部9个主要蜚蠊科的基因组尺度研究，该分析将地鳖蠊科（Corydiidae）与诺氏蠊科（Nocticolidae）聚为一支，并将扁头蜚蠊科（Anaplectidae）置于蜚蠊总科（Blattoidea）其余类群的姊妹分支位置。本研究揭示了诺氏蠊科（Nocticolidae）极高水平的遗传分化，其中包含两个高度分化的支系，二者虽均包含诺氏蠊属（Nocticola）的代表物种，但分化时间约为1.15亿年前。本研究结果凸显了高谱系间速率变异对系统发育关系与进化时间尺度估算的潜在影响。