A non‐monophyly of ‘crowned’ Daphnia (Ctenodaphnia) Dybowski et Grochowski, 1895 (Cladocera: Daphniidae): From genomes to morphology

Daphnia (Crustacea: Cladocera) has been frequently used as a model taxon for studying prey antipredator defences. Among numerous representatives of this genus, there are several taxa within the subgenus Daphnia (Ctenodaphnia) with a morphological innovation unique for these cladocerans, a head plate. In some populations, the margin of this anterior projection of carapace into the head shield is adorned with a remarkable ‘crown of thorns’, which has been shown to be an antipredator adaptation against tadpole shrimps (Notostraca). This structure is phenotypically plastic, dependent on the presence of these omnivorous crustaceans in the respective water bodies. We aimed to evaluate the monophyly of Eurasian ‘crowned’ Daphnia species (i.e., those forming the ‘crown of thorns’ under some circumstance) based on genomic phylogenies and morphology. For this study, we have individually sequenced the genomes of five daphniids, four representing taxa able to form ‘crowns’ (two specimens of different clades of the D. (C.) atkinsoni complex and two specimens of D. (C.) triquetra from distant populations), and D. (C.) mediterranea distantly related to D. (C.) atkinsoni that lacks the head plate. We analysed them along with genomes obtained from GenBank, focusing on either full mitochondrial or partial nuclear datasets (BUSCO). Our main hypothesis on a monophyly of all ‘crowned’ daphnids was rejected. Genomic analyses confirmed existence of two independent lineages able to express this phenotypic trait in the Palaearctic: (1) a monophyletic D. (C.) atkinsoni s. lat. and (2) D. (C.) triquetra, formally redescribed here. These lineages form a well‐supported clade together with several other species lacking a head plate (including D. (C.) mediterranea). Genomic analyses indicate that D. (C.) atkinsoni s. lat. is closely related to D. (C.) tibetana; mitochondrial markers also suggest a close relationship of D. (D.) triquetra with D. (C.) studeri, both D. (C.) tibetana and D. (C.) studeri, are lacking this morphological feature. Molecular clock estimated the time of the differentiation of the major clade containing both ‘crowned Daphnia’ to the Late Mesozoic, confirming an antiquity of the head plate as antipredator defence.