The genome of a daddy-long-legs (Opiliones) illuminates the evolution of arachnid appendages

Chelicerate arthropods exhibit dynamic genome evolution, with ancient whole-genome duplication (WGD) events affecting several orders. Yet, genomes remain unavailable for a number of poorly studied orders, such as Opiliones (daddy-long-legs), which has hindered comparative study. We assembled the first harvestman draft genome for the species Phalangium opilio, which bears elongate, prehensile appendages, made possible by numerous distal articles called tarsomeres. Here, we show that the genome of P. opilio exhibits a single Hox cluster and no evidence of WGD. To investigate the developmental genetic basis for the quintessential trait of this group-the elongate legs-we interrogated the function of the Hox genes Deformed (Dfd) and Sex combs reduced (Scr), and a homologue of Epidermal growth factor receptor (Egfr). Knockdown of Dfd incurred homeotic transformation of two pairs of legs into pedipalps, with dramatic shortening of leg segments in the longest leg pair, whereas homeosis in L3 is only achieved upon double Dfd + Scr knockdown. Knockdown of Egfr incurred shortened appendages and the loss of tarsomeres. The similarity of Egfr loss-of-function phenotypic spectra in insects and this arachnid suggest that repeated cooption of EGFR signalling underlies the independent gains of supernumerary tarsomeres across the arthropod tree of life.

Automated summary

Chelicerate arthropods exhibit dynamic genome evolution, with ancient whole-genome duplication events affecting several orders. The genome of the harvestman Phalangium opilio does not show evidence of whole-genome duplication and contains a single Hox cluster. Functional studies of Hox genes and Egfr in Phalangium opilio reveal their roles in the development of elongate legs and the formation of tarsomeres. The loss of Egfr function in this arachnid species suggests a potential evolutionary mechanism underlying the independent gains of supernumerary tarsomeres in arthropods.