The cat flea (Ctenocephalides felis) is the most common parasite of domestic cats and dogs worldwide. Due to the morphological ambiguity of C. felis and a lack of - particularly largescale - phylogenetic data, we do not know whether global C. felis populations are morphologically and genetically conserved, or whether human-mediated migration of domestic cats and dogs has resulted in homogenous global populations. To determine the ancestral origin of the species and to understand the level of global pervasion of the cat flea and related taxa, our study aimed to document the distribution and phylogenetic relationships of Ctenocephalides fleas found on cats and dogs worldwide. We investigated the potential drivers behind the establishment of regional cat flea populations using a global collection of fleas from cats and dogs across six continents. We morphologically and molecularly evaluated six out of the 14 known taxa comprising genus Ctenocephalides, including the four original C. felis subspecies (Ctenocephalides felis felis, Ctenocephalides felis strongylus, Ctenocephalides felis orientis and Ctenocephalides felis damarensis), the cosmopolitan species Ctenocephalides canis and the African species Ctenocephalides connatus. We confirm the ubiquity of the cat flea, representing 85% of all fleas collected (4357/5123). Using a multigene approach combining two mitochondrial (cox1 and cox2) and two nuclear (Histone H3 and EF-1α) gene markers, as well as a cox1 survey of 516 fleas across 56 countries, we demonstrate out-of-Africa origins for the genus Ctenocephalides and high levels of genetic diversity within C. felis. We define four bioclimatically limited C. felis clusters (Temperate, Tropical I, Tropical II and African) using maximum entropy modelling. This study defines the global distribution, African origin and phylogenetic relationships of global Ctenocephalides fleas, whilst resolving the taxonomy of the C. felis subspecies and related taxa. We show that humans have inadvertently precipitated the expansion of C. felis throughout the world, promoting diverse population structure and bioclimatic plasticity. By demonstrating the link between the global cat flea communities and their affinity for specific bioclimatic niches, we reveal the drivers behind the establishment and success of the cat flea as a global parasite.

Department of Biodiversity University of Limpopo Sovenga 0727 South Africa

Department of Parasitology and Parasitic Diseases Faculty of Veterinary Medicine University of Agricultural Sciences and Veterinary Medicine Cluj Napoca Romania

Department of Parasitology Faculty of Veterinary Medicine Addis Ababa University Debre Zeit Ethiopia

Department of Pathology and Parasitology University of Veterinary and Pharmaceutical Sciences Brno Brno Czech Republic; Biology Centre Institute of Parasitology Czech Academy of Sciences České Budějovice Czech Republic; CEITEC VFU University of Veterinary and Pharmaceutical Sciences Brno Brno Czech Republic

Instituto de Investigaciones en Ciencias de la Salud Universidad Nacional de Asunción Campus UNA San Lorenzo Paraguay

Medical Entomology NSW Health Pathology ICPMR Westmead Hospital Westmead New South Wales 2145 Australia; Marie Bashir Institute of Infectious Diseases and Biosecurity University of Sydney Sydney New South Wales 2006 Australia

School of Veterinary Science The University of Queensland Gatton Queensland Australia; Environmental Futures Research Institute Griffith University Gold Coast Queensland Australia

Sydney School of Veterinary Science Faculty of Science University of Sydney Sydney New South Wales 2006 Australia

Sydney School of Veterinary Science Faculty of Science University of Sydney Sydney New South Wales 2006 Australia; Medical Entomology NSW Health Pathology ICPMR Westmead Hospital Westmead New South Wales 2145 Australia; Marie Bashir Institute of Infectious Diseases and Biosecurity University of Sydney Sydney New South Wales 2006 Australia

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