New taxonomic and evolutionary insights relevant to the cat flea, Ctenocephalides felis: A geographic perspective

The cat flea, Ctenocephalides felis, is an obligate haematophagous ectoparasite of wildlife and domestic cats and dogs worldwide. Since cat fleas can affect the health of humans and their pets, an uncertain taxonomy of this taxon can greatly inhibit pest and disease management. To address the evolution and taxonomy of the cat flea, we set out to determine 1) how many genetically distinct taxa exist, 2) whether there is morphological support for the genetically distinct taxa, and 3) the role of host range and paleoclimatic events in speciation. We collected a total of 3352 fleas sampled from 576 domestic cats and dogs as well as 10 wildlife species across 30 localities in South Africa. A total of three flea genera, five species, and three of the currently recognized cat flea subspecies, C. f. damarensis, C. f. strongylus and C. f. felis were obtained. Geometric morphometric analyses on head shape were performed on 68 female and 107 male cat flea individuals. Principal component analysis demonstrated large overlap in head shape variation between C. f. strongylus and C. f. felis, rendering this character not useful for phylogenetic inferences. DNA was extracted from 188 Ctenocephalides spp. and mitochondrial COII and nuclear EF1-α sequences were generated. Bayesian and Maximum Likelihood analyses as well as a TCS parsimony haplotype network of the mitochondrial DNA confirmed the presence of three well supported monophyletic clades. These assemblages did not fully corroborate the existence of the three C. felis subspecies. A single well-supported molecular clade included only C. f. damarensis morphotypes that were mostly collected from wildlife. The recognition of this subspecies as a distinct taxon was further corroborated by sequence distances and also the number of plantar spiniform bristles on fore-tarsi V in males. Despite the overall lack of support for the recognition of C. f. damarensis and C. f. strongylus, a geographic trend was visible whereby one genetic lineage corresponded to the western dryer hot subregion, whereas the other was found throughout the region. Bayesian dating suggested that these two clades diverged during the early Pliocene (4.18 mya), a date that corresponds well with the establishment of a dry hot climate in the west of southern Africa. If so, the off-host environment, particularly temperature and humidity, are important factors to consider in the evolution of the cat flea. The present study rejects recent assertions that the three cat flea subspecies are valid entities and rather point to a situation where more sampling is required before the taxonomic status of C. f. damarensis can be resolved.