Molecular Phylogeny of Cimicoidea (Heteroptera: Cimicomorpha) Revisited: Increased Taxon Sampling Reveals Evolution of Traumatic Insemination and Paragenitalia

SIMPLE SUMMARY: The superfamily Cimicoidea comprises seven families with more than 600 described species. The members of this group show two feeding habits, predation and blood-feeding, and show the unique hypodermic insemination process called traumatic insemination. A molecular phylogenetic study using increased sampling aimed to hypothesize the phylogenetic relationships within Cimicoidea, and to understand the evolutionary history of traumatic insemination and the correlation between the insemination habit and the morphology, paragenitalia. The phylogenetic results showed that most families within Cimicoidea were confirmed as monophyletic groups and hypothesized the novel sister-group relationship of Curaliidae + Lasiochilidae with high support values. Additionally, it was revealed that at least one shift from standard insemination to traumatic insemination occurred within Cimicoidea, and the acquisition of paragenitalia in cimicoid females was correlated with the traumatic insemination habit. ABSTRACT: The molecular phylogeny of the Cimicoidea was reconstructed from an expanded sampling based on mitochondrial (16S, COI) and nuclear (18S, 28SD3) genes. The data were analyzed using maximum likelihood (ML), maximum parsimony (MP), and Bayesian inference (BI) phylogenetic frameworks. The phylogenetic relationships inferred by the model-based analyses (ML and BI) were largely congruent with those inferred by the MP analysis in terms of the monophyly of most of the higher taxonomic groups and the species-level relationships. The following clades were recovered in all analyses: Cimiciformes; Nabidae: Prostemmatinae; Nabidae: Nabinae; Plokiophilidae; Microphysidae; Lasiochilidae; Cimicidae: Cacodminae; Cimicidae; Lyctocoridae; Anthocoridae s. str.; Cardiastethini excluding Amphiareus; Almeidini; Scolopini; Anthocorini; Oriini; Curaliidae + Lasiochilidae; Almeidini + Xylocorini; Oriini + Cardiastethini; and Anthocorini + Amphiareus. Reconstructions of ancestral copulation states based on Bayesian and parsimony inference indicated that at least one shift from standard insemination (SI) to traumatic insemination (TI) occurred within Cimicoidea, and an investigation of the evolutionary correlation between TI and paragenitalia (PG) revealed that the acquisition of PG in cimicoid females was correlated with the TI habit. Additionally, our morphological examination of various types of PG suggested that even the same PG type may not constitute a homologous feature at various taxonomic levels, indicating the convergent evolution of female morphology to adapt to TI.