| Summary: | Abstract A good knowledge of the evolutionary history of organisms and an accurate taxonomic framework are keys for efficient biodiversity conservation measures. This is particularly relevant for European butterflies, which are often used as bioindicator organisms and umbrella species for conservation. The Holarctic butterfly genus Agriades includes seven European arctic‐alpine species of which several have a debated taxonomic status. They are localized and allopatric, and at least two of them are of high conservation concern, namely A. aquilo (in Europe, restricted to northern Scandinavia) and A. zullichi (endemic to southern Spain). Despite high conservation value and taxonomic uncertainty, molecular studies on these taxa are limited to DNA barcodes. We investigated the evolutionary history and species delimitation of West Palearctic Agriades using double‐digest RAD sequencing (ddRADseq). Various analyses using genomic data suggested the presence of one species in the glandon species group and one or two in the pyrenaicus species group . The differentiation within the former group (i.e., glandon , aquilo , zullichi ) appears to be relatively recent, although the main allopatric populations represent evolutionary significant units (ESUs). Notable geographic structure was found within the pyrenaicus species group, with four allopatric ESUs detected. Wolbachia screening highlighted the presence of several allele combinations, some associated with particular Agriades populations. Genomic data revealed the evolutionary trajectory of European Agriades and a tendency for taxonomic oversplitting within this genus. These findings aid conservation by providing genetic background for region or population prioritization (including ESUs), and for the management of potential population reinforcement or reintroductions.
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