Mitogenomics of Cladocera (Branchiopoda): Marked gene order rearrangements and independent predation roots.

ABSTRACT

Cladocera (Crustacea Branchiopoda) is a key group of invertebrates. Despite a long history of phylogenetic research, relationships within this group remain disputed. We here provide new insights based on 15 new mitochondrial genomes obtained from high-throughput sequencing (HTS) and 40 mitogenomes extracted from published HTS datasets. Together with 25 mitogenomes from GenBank, we generated a matrix of 80 mitogenomes, 44 of them belonging to Cladocera. We also obtained a matrix with 168 nuclear orthologous genes to further assess the phylogenetic result from mitogenomes based on published data and one new HTS data ofLeptodora. Maximum likelihood and Bayesian phylogenetic analyses recovered all Branchiopoda orders as monophyletic and supported a sister-group relationship between Anomopoda and Onychopoda, making the taxon Gymnomera paraphyletic and supporting an independent origin of predatory Haplopoda and Onychopoda. The nuclear phylogeny and topological tests also support Gymnomera as paraphyletic, and the nuclear phylogeny strongly supports a sister-group relationship between Ctenopoda and Haplopoda. We provide a fossil-calibrated time tree, congruent with a Carboniferous origin for Cladocera and a subsequent diversification of the crown group of Anomopoda, Onychopoda, and Ctenopoda, at least in the Triassic. Despite their long evolutionary history, non-Cladoceran Branchiopoda exhibited high mitogenome structural stability. On the other hand, 21 out of 24 gene rearrangements occurred within the relatively younger Cladocera. We found the differential base compositional skewness patterns between Daphnia s.s. and Ctenodaphnia, which might be related to the divergence between these taxa. We also provide evidence to support the recent finding that Spinicaudata possesses mitogenomes with inversed compositional skewness without gene rearrangement. Such a pattern has only been reported in Spinicaudata.