There are calls for research into the historical evolutionary relationships between humans and their commensals, as it would greatly inform models that predict the spread of pests and diseases under urban population expansion. The earliest civilizations emerged approximately 10 000 years ago and created conditions ideal for the establishment and spread of commensal urban pests. Commensal relations between humans and pests likely emerged with these early civilizations; however, for most species (e.g. German cockroach and black rat), these relationships have formed relatively recently-within the last 5000 years-raising the question of whether others could have emerged earlier. Following comparative whole genome analysis of bed bugs, Cimex lectularius, belonging to two genetically distinct lineages, one associated with bats and the other with humans, coupled with demographic modelling, our findings suggests that while their association with humans dates back potentially hundreds of thousands of years, a dramatic change in the effective population size of the human-associated lineage occurred approximately 13 000 years ago; a pattern not found in the bat-associated lineage. The timing and magnitude of the demographic patterns provide compelling evidence that the human-associated lineage closely tracked the demographic history of modern humans and their movement into the first cities. As such, bed bugs may represent the first true urban pest insect species.

• Keywords
• commensal insect, demographic modelling, urban evolution, urbanization, whole genome sequencing,
• MeSH
• Biological Evolution * MeSH
• Chiroptera parasitology   MeSH
• Genome, Insect * MeSH
• Humans MeSH
• Bedbugs * genetics   physiology   MeSH
• Animals MeSH
• Check Tag
• Humans MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH

As populations differentiate across geographic or host-association barriers, interpopulation fertility is often a measure of the extent of incipient speciation. The bed bug, Cimex lectularius L., was recently found to form two host-associated lineages within Europe: one found with humans (human-associated, HA) and the other found with bats (bat-associated, BA). No unequivocal evidence of contemporary gene flow between these lineages has been found; however, it is unclear whether this is due to an inability to produce viable "hybrid" offspring. To address this question and determine the extent of compatibility between host-associated lineages, we set up mating crosses among populations of bed bugs based on both their host association (human-HA vs. bat-BA) and geographic origin (North America vs. Europe). Within-population fecundity was significantly higher for all HA populations (>1.7 eggs/day) than for BA populations (<1 egg/day). However, all within-population crosses, regardless of host association, had >92% egg hatch rates. Contrary to previous reports, in all interlineage crosses, successful matings occurred, fertile eggs were oviposited, and the F1 "hybrid" generation was found to be reproductively viable. In addition, we evaluated interpopulation genetic variation in Wolbachia among host-associated lineages. We did not find any clear patterns related to host association, nor did we observe a homogenization of Wolbachia lineages across populations that might explain a breakdown of reproductive incompatibility. These results indicate that while the HA and BA populations of C. lectularius represent genetically differentiated host-associated lineages, possibly undergoing sympatric speciation, this is in its incipient stage as they remain reproductively compatible. Other behavioral, physiological, and/or ecological factors likely maintain host-associated differentiation.

• Keywords
• Cimexlectularius, Wolbachia, host‐associated differentiation, reproduction, speciation,
• Publication type
• Journal Article MeSH