The effect of host vicariance and parasite life history on the dispersal of the multi‐host ectoparasite, Hyalomma truncatum

Abstract

Aim It is predicted that the dispersal and gene flow of ectoparasites with wide host ranges are correlated with the vagilities of their most mobile hosts. To test this, the phylogeographical structure of a widespread generalist tick occurring on large ungulates was determined and compared with previously published host patterns. Location Africa. Methods mtDNA cytochrome c oxidase subunit I (COI) sequences were generated for 182 Hyalomma truncatum specimens sampled from 21 Afrotropical localities. A subsample of these was sequenced for the nuclear Histone 3 (H3) and Calreticulin (CRT) regions. Phylogeographical inferences were made by using haplotype networks, a Bayesian analysis of population structure, isolation by distance (IBD) and a Bayesian gene tree. Demographic changes in the populations were determined with Bayesian skyline plots. Results Two highly divergent geographically confined mtDNA clades were detected, and these were partly supported by significant differentiation at nuclear DNA level. The clades differ by 9.88% (± 0.40%) mtDNA COI sequence divergence. The southern African clade, which expanded approximately 100 ka, shows no geographical barriers to dispersal and also no IBD. The northern African clade shows signs of IBD, at least five distinct genetic subgroups and an earlier expansion at 200 ka. Conclusion The phylogeography of the generalist tick is broadly congruent with host vicariance and supports the previously defined African Pleistocene savanna refugia. The magnitude of the sequence divergence between geographically separated genetic lineages suggests that H. truncatum comprises two distinct yet undescribed species. The dispersal of ectoparasites with wide host ranges is dependent on the ability of the various life stages of the parasite to survive in the off‐host environment coupled to host movement.

Comparative phylogeography of parasitic Laelaps mites contribute new insights into the specialist-generalist variation hypothesis (SGVH)

“…(hosts for specialist mites) show a much higher average level of mtDNA population differentiation (F st = 0.95, P < 0.05) when compared to M. coucha (most mobile hosts for the generalist mite) (F st = 0.36, P < 0.05). Although the data here support the paradigm that parasite genetic structure depends on host dispersal [ 42 ], it is well documented that parasite life history [ 14 , 43 , 44 ] and abiotic factors [ 45 ] can equally influence parasite population differentiation. Since the majority of life history characteristics of the two Laelaps species used in our study are very similar [ 6 , 23 ], and both species were most likely exposed to similar abiotic factors in their overlapping ranges (with eight identical sampling localities), we can most likely attribute the differences in population genetic structure of the parasites to either differences in life histories of the hosts, host dispersal ability, or species specificity of the parasite (or a combination of these three).…”

The influence of host dispersal on the gene flow and genetic diversity of generalist and specialist ectoparasites

“…To limit some of the tribulations associated with F st comparisons among species (Willing et al 2012;Sovic et al 2019), all these parasite taxa were represented by a reasonably large number of individuals (97-278; Table 1) and populations (6-25; Table 1), they were sampled in the same geographic region, and the COI and COII mtDNA molecular markers used show no dramatic intergene variability (Lopez et al 1997). Three generalist (parasites completing their life cycle on multiple host species) tick species (Amblyomma hebraeum, Hyalomma truncatum, Hyalomma rufipes) that represent temporary parasites (parasites that are free-living during part of their life cycle) and whose adult stages commonly also occur on large mobile antelope and domestic ungulates (Cangi et al 2013;Sands et al 2017) are compared with two semi-permanent (parasites that utilise a host at one or more life stages, but some life stages are free living) generalist flea species (Listropsylla agrippinae, Chiastopsylla rossi) that exclusively occur on small rodents, shrews, and elephant shrews (Table 1; van der Mescht et al 2015). Compared with the hosts of the tick taxa, the hosts of the flea species are less mobile; if host vagility is an important factor in parasite dispersion, then larger population differentiation values are expected for the fleas that occur on less mobile hosts.…”

“…All sequence data were included from the published studies except in two instances. Hyalomma truncatum is a widely distributed species throughout Africa and show considerable population differentiation at the continental level (Sands et al 2017) and in this instance only individuals in the southern African clade were included. In the case of Polyplax arvicanthis, two cryptic species with similar genetic patterns were detected and only lineage 2 (the most comprehensively sampled clade) was included (du Toit et al 2013).…”

Tandem host‐parasite dispersal inferred from similarities in phylogeographical patterns among Little Penguins and their ‘terrestrial’ ectoparasites

“…the extent of free-living stages, see Mazé-Guilmo, Blanchet, McCoy, & Loot, 2016 for a review), and in the case of ectoparasites, some of which show looser associations with host species than endoparasites (e.g. those with considerable off-host phases, and multi-host lifecycles), comparison of host-parasite phylogeographical and/or phylogenetic structure has been less commonly undertaken (but see Sands, Apanaskevich, Matthee, Horak, & Matthee, 2017;Talbot, Vonhof, Broders, Fenton, & Keyghobadi, 2016).…”