Integrating phylogenomic and population genomic patterns in avian lice provides a more complete picture of parasite evolution

Abstract

Parasite diversity accounts for most of the biodiversity on earth, and is shaped by many processes (e.g., cospeciation, host switching). To identify the effects of the processes that shape parasite diversity, it is ideal to incorporate both deep (phylogenetic) and shallow (population) perspectives. To this end, we developed a novel workflow to obtain phylogenetic and population genetic data from whole genome sequences of body lice parasitizing New World ground-doves. Phylogenies from these data showed consistent, highly resolved species-level relationships for the lice. By comparing the louse and ground-dove phylogenies, we found that over long-term evolutionary scales their phylogenies were largely congruent. Many louse lineages (both species and populations) also demonstrated high host-specificity, suggesting ground-dove divergence is a primary driver of their parasites' diversity. However, the few louse taxa that are generalists are structured according to biogeography at the population level. This suggests dispersal among sympatric hosts has some effect on body louse diversity, but over deeper time scales the parasites eventually sort according to host species. Overall, our results demonstrate that multiple factors explain the patterns of diversity in this group of parasites, and that the effects of these factors can vary over different evolutionary scales. The integrative approach we employed was crucial for uncovering these patterns, and should be broadly applicable to other studies.

Cophylogenetic assessment of New World warblers (Parulidae) and their symbiotic feather mites (Proctophyllodidae)

“…Geography may also help explain the patterns of likely host switching that we uncovered (similar to avian lice studied in Weckstein 2004, Sweet and Johnson 2016, Catanach et al 2017, Sweet et al 2017). The hosts we studied vary in their geographic overlap during different stages of their annual cycle (breeding, migration, non-breeding;Stephenson and Whittle 2013).…”

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

“…We obtained additional raw genomic read data from ncbi's sra database for five in‐group (SRR3161921‐SRR3161923, SRR3161930‐SRR3161931) and four out‐group Columbicola taxa ( C. columbae : SRR3161917, C. gracilicapitis : SRR3161913, C. macrourae : SRR3161953, C. veigasimoni : SRR3161919) (Boyd et al, ). We also obtained raw sequence reads for 34 body louse individuals ( Physconelloides ) from the SRA database (SRP076185) (Sweet et al, ). These data represent all described ground‐dove wing and body louse species, several potential cryptic species and most host species and biogeographic areas (Supporting Information Table ).…”

“…To assemble nuclear loci from genomic reads, we used an approach similar to the one detailed in Sweet et al (), which maps lower coverage, multiplexed genomic data to reference loci from a closely related taxon. For our reference set of nuclear loci for wing lice, we used 1,039 exons of Columbicola drowni generated in Boyd et al () (raw data: SRR3161922).…”

“…Here, we focus on the wing and body lice of small‐bodied New World ground‐doves, a monophyletic group of 17 dove species distributed from the southern United States to southern South America (Gibbs, Cox, & Cox, ; Pereira, Johnson, Clayton, & Baker, ; Sweet & Johnson, ). There are three described species of both wing (genus Columbicola ) and body lice (genus Physconelloides ) on this host group, although there are likely additional cryptic species (Price, Hellenthal, Palma, Johnson, & Clayton, ; Sweet & Johnson, ; Sweet et al, ). Both types of lice also form monophyletic groups within their respective genera (Johnson et al, ), which makes interpretation of evolutionary history straightforward.…”

“…Both types of lice also form monophyletic groups within their respective genera (Johnson et al, ), which makes interpretation of evolutionary history straightforward. Obtaining genomic‐level data is very feasible for these lice, as recently published genomic studies on avian lice have established pipelines for assembling data appropriate for both phylogenetic and population genetic analysis (Allen et al, ; Boyd et al, ; Sweet et al, ).…”