Papadopoulos Nikolaos, Kulkarni Siddharth S, Baranyi Christian, Fromm Bastian, Setton Emily V W, Sharma Prashant P, Wanninger Andreas, Brenneis Georg
Integrative Zoology Unit, Department of Evolutionary Biology, University of Vienna, Vienna, Austria.
CSIR-Centre for Cellular and Molecular Biology, Hyderabad, India.
BMC Biol. 2025 Jul 2;23(1):196. doi: 10.1186/s12915-025-02276-x.
Chelicerate evolution is contentiously debated, with recent studies challenging traditional phylogenetic hypotheses and scenarios of major evolutionary events, like terrestrialization. Sea spiders (Pycnogonida) represent the uncontested marine sister group of all other chelicerates, featuring a-likely plesiomorphic-indirect development. Accordingly, pycnogonids hold the potential to provide crucial insight into the evolution of chelicerate genomes and body patterning. Due to the lack of high-quality genomic and transcriptomic resources, however, this potential remains largely unexplored.
We employ long-read sequencing and proximity ligation data to assemble the first near chromosome-level sea spider genome for Pycnogonum litorale, complemented by comprehensive transcriptomic resources. The assembly has a size of 471 Mb in 57 pseudochromosomes, a repeat content of 61.05%, 15,372 predicted protein-coding genes, and robust completeness scores (95.8% BUSCO Arthropoda score, 95.7% of conserved microRNA families). Genome-scale self-synteny and homeobox gene cluster analysis show no evidence of a whole-genome duplication (WGD). We identify a single, intact Hox cluster lacking Abdominal-A (abdA/Hox9), corroborated by the absence of an abdA ortholog in the novel transcriptomic resources.
Our high-quality genomic and transcriptomic resources establish P. litorale as a key research organism for modern studies on chelicerate genome evolution, development, and phylogeny. The lack of WGD signature in P. litorale further strengthens the inference that WGDs are derived traits in the chelicerate tree. The combination of abdA loss with the reduction of the posterior tagma emerges as a common theme in arthropod evolution, as it is shared with other, distantly related arthropod taxa with a vestigial opisthosoma/abdomen.
螯肢动物的进化存在激烈争论，近期研究对传统系统发育假说以及陆地化等重大进化事件的情景提出了挑战。海蜘蛛（海蛛纲）是所有其他螯肢动物无可争议的海洋姐妹类群，具有一种可能是近祖型的间接发育方式。因此，海蜘蛛有潜力为螯肢动物基因组和身体模式的进化提供关键见解。然而，由于缺乏高质量的基因组和转录组资源，这一潜力在很大程度上尚未得到探索。
我们利用长读长测序和邻近连接数据，为滨海海蛛组装了首个接近染色体水平的海蜘蛛基因组，并辅以全面的转录组资源。该组装体大小为471兆碱基，分布在57条假染色体上，重复序列含量为61.05%，预测有15372个蛋白质编码基因，且完整性得分较高（节肢动物BUSCO得分95.8%，保守微小RNA家族的95.7%）。基因组规模的自同线性和同源框基因簇分析表明没有全基因组复制（WGD）的证据。我们鉴定出一个单一的、完整的缺少腹部A（abdA/Hox9）的Hox簇，新的转录组资源中没有abdA直系同源物也证实了这一点。
我们的高质量基因组和转录组资源使滨海海蛛成为现代螯肢动物基因组进化、发育和系统发育研究的关键研究生物体。滨海海蛛中缺乏WGD特征进一步强化了WGD是螯肢动物谱系中衍生特征的推断。abdA缺失与后体节减少的结合成为节肢动物进化中的一个共同主题，因为它与其他具有退化后体躯/腹部的远缘节肢动物类群相同。
