Origin and Biogeography of the Colourful Sap‐Sucking Sea Slugs Genus <i>Thuridilla</i> Bergh, 1872 (Mollusca, Gastropoda, Heterobranchia)

ABSTRACT Aim Thuridilla Bergh, 1872, is a lineage of herbivorous sea slugs externally distinguished by bright colours and distinctive patterns of lines and spots. Recent work revealed an exceptionally rapid, cryptic radiation of 13 species in the Indo‐Pacific, raising questions about mechanisms of speciation in this group. Here, we (i) study the diversification and historical biogeography of Thuridilla in a phylogenetic context and (ii) assess the role of dispersal and vicariance as the predominant mode of speciation in the genus. Location Tropical and temperate regions of the Atlantic and Indo‐Pacific. Major Taxa Studies Gastropoda, Sacoglossa. Methods A nearly complete taxon set with 28 out of 32 recognised species of Thuridilla was used, in a total sample of 172 specimens, together with sacoglossan outgroups. Phylogenetic relationships were determined using a multi‐locus approach combining two mitochondrial (COI and 16S) and one nuclear gene (H3). Species relationships, diversification times, and ancestral geographical ranges were inferred using relaxed‐clock methods together with Bayesian discrete phylogeographic methods under three calibration scenarios using the oldest known fossil of Sacoglossa, Berthelinia elegans Crosse, 1875, and tectonic events. Results Thuridilla species branched off into four major clades in all calibration scenarios: two groups from the Atlantic plus Indo‐West Pacific (5 and 6 species) and two clades from the Indo‐West Pacific (4 and 17 species). The highest diversity of the genus is in the Western Pacific (14 spp.) with a peak in the East Indies Triangle (18 spp.), whereas the Atlantic is depauperate with only four species occurring in this ocean basin. Divergence between Atlantic and Indo‐West Pacific lineages occurred in two main temporal periods: the Miocene and the Pliocene. Speciation events within the 13 cryptic species‐complex fell mostly within Plio‐Pleistocene times. Main Conclusions The best supported hypothesis was an Indo‐West Pacific origin of Thuridilla between 28 and 18 Mya during the Early Miocene. In the western Pacific, speciation likely occurred during transient allopatry during Plio‐Pleistocene sea‐level fluctuations. Under the three tested calibration scenarios, the limited diversity of the Atlantic Ocean is hypothesized to be derived from Miocene vicariant events associated with the closure of the Tethys Sea, dispersal across southern Africa, or long‐distance dispersal across the East Pacific Barrier prior to the uplift of the Isthmus of Panama. Thuridilla is absent in the Eastern Pacific, potentially resulting from the extinction of ancestral lineages following the uplift of the Isthmus of Panama. Near‐complete sampling of diversity and reconstruction of historical biogeography thus yielded new insight into the relative contributions of dispersal versus vicariance during speciation over the history of this widely distributed, colourful genus.