Late Cenozoic environmental changes drove the diversification of a weevil genus endemic to the Cape Floristic Region

We thank the Western Cape Nature Conservation Board (permit No. CN44-30-4229), the Cape Research Centre (South African National Parks, CRC/2019-2020/012-2012/V1) and Grootbos Private Nature reserve for authorization to collect specimens in the Western Cape province of South Africa.; International audience; The Cape Floristic Region in the Republic of South Africa is a well-recognized hotspot of biodiversity. Although this region is mostly known for its high level of plant diversity and endemicity, it also hosts an understudied and likely diverse arthropod fauna. Here we investigate the evolutionary history and timing of diversification of the apterous weevil genus Phlyctinus (Curculionidae: Entiminae), which is endemic to the coastal area and adjacent mountain ranges of the Cape floristic region and generally associated with sunflower plants (Asteraceae). We use a diverse array of molecular analyses (phylogenetic inference, molecular species delimitation and dating analyses) to analyse a novel molecular dataset of 202 weevil specimens (including 170 Phlyctinus sampled in 60 sites), and sequenced for two mitochondrial and four nuclear gene fragments. Phylogenetic and dating analyses indicate that the genus started diversifying in the late Miocene, with contrasting diversification dynamics for the three inferred clades, which present disjunct distributions. Host plant records and the lack of relatedness of species living in sympatry indicate that the diversification of Phlyctinus was predominantly driven by allopatric (geographic) speciation. We hypothesize that the interplay between topography and recurring cycles of coastline-habitat fragmentation resulting from sea level oscillations spurred the diversification of the most speciose clade, whereas in the two remaining clades populations likely remained connected thus hampering allopatric speciation. Interestingly, this pattern echoes with the role of sea level oscillations as an important driver of the radiation of several lineages in the coastline ecosystems of the Cape Floristic Region.