Phylogenomics and biogeography of North American Trechine cave beetles (Coleoptera: Carabidae)

Cave trechines beetles (Coleoptera: Carabidae: Trechini) are members of cave communities globally and important models for understanding the colonization of caves, adaptation to cave life, and the diversification of cave-adapted lineages. In eastern North America, cave trechines are the most species-rich group of terrestrial troglobionts, hypothesized to comprise over 150 taxa in six genera with no extant surface members. Previous studies have hypothesized that the Pleistocene climate change was a major driver of cave colonization and diversification in the temperate terrestrial cave fauna in this region. However, our time-calibrated molecular phylogeny resulting from the analysis of 16,794 bases from 68 Ultraconserved Elements (UCEs) loci for 45 species of the clade supports an alternative hypothesis whereby cave colonization of the surface ancestor of eastern North American cave trechines likely began in the early Miocene in the Appalachians Ridge and Valley (APP) and dispersed into the Interior Low Plateau (ILP) in an east to west manner beginning 17.0 Mya. The APP served as a cradle for diversification and as a bridge linking the southern Appalachians and Interior Low Plateau enabling the dispersal and subsequent diversification of this cave beetles. Major clades in our time-calibrated phylogeny attained their present-day geographic distributions by the early Miocene followed by multiple additional episodes of cave colonization and diversification occurring throughout the Pliocene and Pleistocene. The genera Neaphanops, Darlingtonea, Nelsonites, and Ameroduvalius were nested within speciose genus Pseudanophthalmus supporting the hypothesis that these taxa are derived Pseudanophthalmus. Moreover, while several morphologically-defined species groups of Pseudanophthalmus were recovered as monophyletic, others were not warranting future taxonomic and systematic research. The molecular systematics and biogeography of these unique trechine cave beetles offer a model for other comparative evolutionary and ecological studies of troglobionts to further our understanding of factors driving speciation and biogeographic patterns.

洞穴条甲族步甲（鞘翅目Coleoptera: 步甲科Carabidae: 条甲族Trechini）是全球洞穴群落的组成类群，同时亦是探究洞穴定殖、洞穴生活适应性以及洞穴适应支系多样化过程的核心模式类群。在北美东部地区，洞穴条甲族步甲是物种多样性最高的陆生洞穴专生生物（troglobionts），被推测包含6个属的150余个分类单元，且无现生地表类群。此前的研究曾提出，更新世气候变化是该区域温带陆生洞穴动物类群洞穴定殖与多样化的主要驱动因素。本研究针对该演化支的45个物种，对68个超保守元件（Ultraconserved Elements, UCEs）位点的16794个碱基序列开展分析，构建了时间校准的分子系统发育树，结果支持了另一全新假说：北美东部洞穴条甲族步甲的地表祖先类群的洞穴定殖事件最早发生于中新世早期的阿巴拉契亚岭谷区（APP），并于1700万年前以自东向西的扩散模式进入内陆低高原（ILP）。阿巴拉契亚岭谷区既是该类群多样化的演化摇篮，亦是连接南阿巴拉契亚与内陆低高原的地理桥梁，助力此类洞穴步甲完成跨区域扩散与后续的多样化进程。本研究的时间校准系统发育树显示，主要演化支在中新世早期便已形成现今的地理分布格局，随后在整个上新世与更新世期间又发生了多轮洞穴定殖与多样化事件。系统发育分析结果显示，Neaphanops、Darlingtonea、Nelsonites与Ameroduvalius这四个属嵌套于物种丰富的伪盲步甲属（Pseudanophthalmus）之中，支持了这些类群均由伪盲步甲属衍生而来的分类假说。此外，尽管伪盲步甲属的多个基于形态学定义的物种群被恢复为单系群，但其余类群并不满足单系性，这一结果亟需未来开展针对性的分类学与系统学研究予以厘清。此类独特的洞穴条甲族步甲的分子系统学与生物地理学研究，可为其他洞穴专生生物的比较进化与生态学研究提供标准化参照模型，以进一步深化我们对驱动物种形成与生物地理格局形成的关键因素的认知。