Genetic identification and population structure of ectoparasites infesting endemic South African rodents

Abstract

Fleas (Siphonaptera) are specialized and cosmopolitan ectoparasites that parasitize birds and mammals. Morphological variation of fleas makes their identification based on morphological features alone difficult, requiring trained experts. Employing a broadly worldwide dataset of DNA barcodes has been proposed as a quick and reliable tool for the identification of species that does not require taxonomic expertise. However, currently, no information is available for the identification of many species using molecular markers. This is particularly true for African fleas. Fleas differ in their life history traits (e.g., host-specificity and microhabitat preferences, and in being a fur versus a nest flea), which can also shape their genetic structure. There are notable gaps on the dispersal abilities and population structures of South African fleas, particularly when they infest the same host. The Namaqua rock mouse (Micaelamys namaquensis) is an endemic African host of three co-infesting fleas including, Xenopsylla brasiliensis, Chiastopsylla godfreyi, and Epirimia aganippes. While the fur flea, X. brasiliensis is a generalist flea of African origin with a cosmoplitan distribution, the other two have a much narrower host range and use M. namaquensis as their primary host. However, while C. godfreyi is a nest flea; E. aganippes is considered a fur flea. This study aimed to provide a morphological characterization and molecular-based barcodes of cytochrome C oxidase subunit I (COI) marker for these fleas from Telperion/Ezemvelo Nature Reserve in Gauteng Province, South Africa. Additionally, the study investigated how host-specificity and microhabitat preference may affect fine-scale population genetic structure and gene flow of these flea species. The study provides a re-description of the morphological features of the three flea species and augments their known descriptions with additional morphological measurements. All flea species exhibited a sexual size dimorphism with females being considerably larger than males. This is most likely related to female fecundity. This study provides the first COI barcodes of two endemic southern African fleas and new DNA sequences for X. brasiliensis in South Africa. The findings of this study revealed that the generalist fur flea, X. brasiliensis had the greatest genetic diversity and lacked genetic differentiation. Analysis of molecular variance (AMOVA) verified the presence of genetic structuring among the study plots for E. aganippes, and it was the most host-specific of the three flea species studied and showed spatial genetic structure. Chiastopsylla godfreyi on the other hand although presumed to have only a slighter wider host range, had a moderate COI haplotype and nucleotide diversity, suggesting the existence of connectivity among populations at the sampling sites. It furthermore could be an indication of a larger host range than is currently known. Through the collection of three flea species, the study was able to investigate the contrasting patterns of gene flow in the three fleas which showed that variable degrees of genetic structure exists. This study with the application of DNA barcoding provides novel data on the role of host-specificity and microhabitat choice in shaping the genetic structure of flea species with different life history traits. It also highlights that genetic pattern studies should be established to understand the importance of life history traits for fleas.