Abstract
All 100+ bedbug species (Cimicidae) are obligate blood-sucking parasites and well-known for their habit of traumatic insemination but the evolutionary trajectory of these characters is unknown. Our new, fossil-dated, molecular phylogeny estimates that ancestral Cimicidae evolved ca. 115MYA as hematophagous specialists on an unidentified host, 50MY before bats, switching to bats and birds thereafter. Humans were independently colonized three times and our phylogeny rejects the idea that the divergence of the two current urban pests (Cimex lectularius and C. hemipterus) 47MYA was associated with the divergence of Homo sapiens and H. erectus (1.6MYA). The female’s functional reproductive tract is unusually diverse and heterotopic, despite the unusual and strong morphological stasis of the male genitalia. This sex-reversal in genital co-variation is incompatible with current models of genital evolution. The evolutionary trait diversification in cimicids allowed us to uncover fascinating biology and link it to human pre-history and current activity.