Phoretic dispersal influences parasite population genetic structure

Abstract

Dispersal is a fundamental component of the life history of most species. Dispersal influences fitness, population dynamics, gene flow, genetic drift and population genetic structure. Even small differences in dispersal can alter ecological interactions and trigger an evolutionary cascade. Linking such ecological processes with evolutionary patterns is difficult, but can be carried out in the proper comparative context. Here, we investigate how differences in phoretic dispersal influence the population genetic structure of two different parasites of the same host species. We focus on two species of host-specific feather lice (Phthiraptera: Ischnocera) that co-occur on feral rock pigeons (Columba livia). Although these lice are ecologically very similar, "wing lice" (Columbicola columbae) disperse phoretically by "hitchhiking" on pigeon flies (Diptera: Hippoboscidae), while "body lice" (Campanulotes compar) do not. Differences in the phoretic dispersal of these species are thought to underlie observed differences in host specificity, as well as the degree of host-parasite cospeciation. These ecological and macroevolutionary patterns suggest that body lice should exhibit more genetic differentiation than wing lice. We tested this prediction among lice on individual birds and among lice on birds from three pigeon flocks. We found higher levels of genetic differentiation in body lice compared to wing lice at two spatial scales. Our results indicate that differences in phoretic dispersal can explain microevolutionary differences in population genetic structure and are consistent with macroevolutionary differences in the degree of host-parasite cospeciation.

The role of parasite dispersal in shaping a host–parasite system at multiple evolutionary scales

“…The ability of wing lice to disperse between different host individuals provides an opportunity for multiple populations to maintain gene flow. Because body lice have more limited opportunities for dispersal, they can become isolated on a host population or individual, thus leading to lower heterozygosity and more inbred louse populations (DiBlasi et al, ; Koop et al, ; Nadler, ). However, when examining patterns in heterozygosity in more detail, the overall pattern seems to be driven by differences in heterozygosity for host specialists (i.e., species of lice associated with a single host species).…”

“…Clayton and Johnson () showed that wing lice have little cospeciation with their hosts and high levels of host switching compared to body lice from the same host species. Focusing within a louse species, Johnson, Williams, Drown, Adams, and Clayton () and DiBlasi et al () demonstrated that wing lice have less population genetic structure than body lice. To build on this work, an ideal approach would integrate both phylogenetic and population genetic patterns for the same louse taxa, thus simultaneously providing macro‐ and microevolutionary perspectives of the pigeon and dove louse system.…”

“…In particular, we predict that body lice should show more population genetic structure among host species than wing lice (Johnson et al, ), but not necessarily more population structure among biogeographic regions. Dispersal may also contribute to genetic structure between louse populations (infrapopulations) on different host individuals of the same host species (DiBlasi et al, ; Koop, DeMatteo, Parker, & Whiteman, ). In this case, because dispersal is likely to be more limited for body lice, their infrapopulations are more likely to be highly inbred (Nadler, ).…”

Comparing rates of introgression in parasitic feather lice with differing dispersal capabilities

“…Organisms differ in their dispersal abilities, and these differences have an impact on their biology, such as on the distributional range of a species or gene flow between populations (Bohonak 1999). For example, organisms with lower dispersal abilities tend to have smaller distributional ranges and populations that are genetically more structured (Bohonak 1999;Dawson et al 2014;DiBlasi et al 2018).…”

“…Testing for the effect of dispersal on hybridization should ideally hold constant most factors other than dispersal. The ecological replicate system of wing and body lice (Insecta: Phthiraptera) of pigeons and doves (Aves: Columbidae) has proven to be an ideal system for comparing the impact of dispersal differences on other aspects of biology, such as population structure and codivergence (Clayton and Johnson 2003;Johnson and Clayton 2004;Clayton et al 2015;DiBlasi et al 2018;Sweet and Johnson 2018). Specifically, this is an excellent system in which to assess the effect of differences in dispersal capabilities on levels of introgression because both of these lineages of feather lice: 1) significantly differ in their dispersal ability (Harbison et al 2008(Harbison et al , 2009Bartlow et al 2016), 2) co-occur across the diversity of pigeons and doves, and 3) have the same basic life history and diet (Clayton et al 2015;Johnson 2015, 2018).…”