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

Abstract

BackgroundThe specialist-generalist variation hypothesis (SGVH) in parasites suggests that, due to patchiness in habitat (host availability), specialist species will show more subdivided population structure when compared to generalist species. In addition, since specialist species are more prone to local stochastic extinction events with their hosts, they will show lower levels of intraspecific genetic diversity when compared to more generalist.ResultsTo test the wider applicability of the SGVH we compared 337 cytochrome oxidase I mitochondrial DNA and 268 nuclear tropomyosin DNA sequenced fragments derived from two co-distributed Laelaps mite species and compared the data to 294 COI mtDNA sequences derived from the respective hosts Rhabdomys dilectus, R. bechuanae, Mastomys coucha and M. natalensis. In support of the SGVH, the generalist L. muricola was characterized by a high mtDNA haplotypic diversity of 0.97 (±0.00) and a low level of population differentiation (mtDNA Fst = 0.56, p < 0.05; nuDNA Fst = 0.33, P < 0.05) while the specialist L. giganteus was overall characterized by a lower haplotypic diversity of 0.77 (±0.03) and comparatively higher levels of population differentiation (mtDNA Fst = 0.87, P < 0.05; nuDNA Fst = 0.48, P < 0.05). When the two specialist L. giganteus lineages, which occur on two different Rhabdomys species, are respectively compared to the generalist parasite, L. muricola, the SGVH is not fully supported. One of the specialist L. giganteus species occurring on R. dilectus shows similar low levels of population differentiation (mtDNA Fst = 0.53, P < 0.05; nuDNA Fst = 0.12, P < 0.05) than that found for the generalist L. muricola. This finding can be correlated to differences in host dispersal: R. bechuanae populations are characterized by a differentiated mtDNA Fst of 0.79 (P < 0.05) while R. dilectus populations are less structured with a mtDNA Fst = 0.18 (P < 0.05).ConclusionsThese findings suggest that in ectoparasites, host specificity and the vagility of the host are both important drivers for parasite dispersal. It is proposed that the SGHV hypothesis should also incorporate reference to host dispersal since in our case only the specialist species who occur on less mobile hosts showed more subdivided population structure when compared to generalist species.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1245-7) contains supplementary material, which is available to authorized users.

Divergent mitochondrial lineages arose within a large, panmictic population of the Savannah sparrow (Passerculus sandwichensis)

“…Second, the specialist–generalist variation hypothesis posits that more specialized species will exhibit greater population structure, lower levels of gene flow and lower genetic diversity relative to generalist species (Li, Jovelin, Yoshiga, Tanaka, & Cutter, ). Although this hypothesis has received mixed support (e.g., Hung, Drovetski, & Zink, ; Matthee, Engelbrecht, & Matthee, ; Titus & Daly, ), a generalist ecology likely contributes to the lack of population genetic structure and large effective population sizes observed within nominate Savannah sparrows. Savannah sparrows occupy a diversity of open habitats ranging from tundra to salt marshes to agricultural fields (Wheelwright & Rising, ).…”

“…). Although this hypothesis has received mixed support (e.g.,Hung, Drovetski, & Zink, 2017;Matthee, Engelbrecht, & Matthee, 2018;Titus & Daly, 2017), a generalist ecology likely contributes to the lack of population genetic structure and large effective popula-…”

Who Is Dermanyssus gallinae? Genetic Structure of Populations and Critical Synthesis of the Current Knowledge

“…To solve this problem, Roy et al (2,4) took advantage of the recurrent presence of heterozygous indels (indels of fixed 3-7-bp sequences) across the intron n to separate the two alleles of each heterozygous individual, as follows: (i) mapping of these indels based on sequence alignment of homozygous individuals allowed the definition of internal primers targeting the alleles with and without the different indels; (ii) the first heterozygous indel in each of the two directions was located on chromatograms from heterozygous individuals; (iii) two new sequencing reactions were conducted in each direction for each heterozygous individual to obtain the totality of the sequences of each allele. Although, somewhat tedious and expensive, this procedure has allowed refining the use of a nuclear marker to assess interspecific boundaries and to clarify the phylogenetic relationships within the genus Dermanyssus (19), but also to explore the genetic structure of D. gallinae populations (4) as well as, more recently, the genetic structure of mesostigmatic mite species belonging to the family Laelapidae (41).…”

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

“…Through comparative phylogeographic studies between parasites and their hosts, it is evident that differences in parasite abundances on the hosts (Engelbrecht et al 2016), ecological interactions between parasites (Cangi et al 2013), and biogeographic conditions (Dick and Patterson 2007;du Toit et al 2013; van der Mescht et al 2015;Martinů et al 2018;Stefan et al 2018), can synergistically or separately all play a role in the dispersal and subsequent evolution of parasites. Given the close association between parasites and their hosts, and the fact that most terrestrial ectoparasite species are intrinsically not highly mobile, it is reasonable to suggest that host vagility will be a major contributing factor to facilitate parasite gene flow in terrestrial environments (Blasco-Costa, Waters and Poulin 2012;Araya-Anchetta et al 2015;Matthee et al 2018). In addition to host dispersal abilities, the life history of parasites and specifically also the host range (generalist or specialist) is probably equally important from an evolutionary point of view.…”

“…In addition to host dispersal abilities, the life history of parasites and specifically also the host range (generalist or specialist) is probably equally important from an evolutionary point of view. Specialist parasites (those that can only survive on members of a single host species) often show more impediments to gene flow (high levels of genetic structure) and also often low levels of genetic diversity, a scenario best explained by the Specialist Generalist Variation Hypothesis (SGVH;Li et al 2014;Matthee et al 2018). The SGVH suggests that impediments to gene flow result from a lower prevalence of parasite habitat (host availability is less in host specific…”