Nuclear genetic diversity in human lice (Pediculus humanus) reveals continental differences and high inbreeding among worldwide populations

Abstract

Understanding the evolution of parasites is important to both basic and applied evolutionary biology. Knowledge of the genetic structure of parasite populations is critical for our ability to predict how an infection can spread through a host population and for the design of effective control methods. However, very little is known about the genetic structure of most human parasites, including the human louse (Pediculus humanus). This species is composed of two ecotypes: the head louse (Pediculus humanus capitis De Geer), and the clothing (body) louse (Pediculus humanus humanus Linnaeus). Hundreds of millions of head louse infestations affect children every year, and this number is on the rise, in part because of increased resistance to insecticides. Clothing lice affect mostly homeless and refugee-camp populations and although they are less prevalent than head lice, the medical consequences are more severe because they vector deadly bacterial pathogens. In this study we present the first assessment of the genetic structure of human louse populations by analyzing the nuclear genetic variation at 15 newly developed microsatellite loci in 93 human lice from 11 sites in four world regions. Both ecotypes showed heterozygote deficits relative to Hardy-Weinberg equilibrium and high inbreeding values, an expected pattern given their parasitic life history. Bayesian clustering analyses assigned lice to four distinct genetic clusters that were geographically structured. The low levels of gene flow among louse populations suggested that the evolution of insecticide resistance in lice would most likely be affected by local selection pressures, underscoring the importance of tailoring control strategies to population-specific genetic makeup and evolutionary history. Our panel of microsatellite markers provides powerful data to investigate not only ecological and evolutionary processes in lice, but also those in their human hosts because of the long-term coevolutionary association between lice and humans.

Figure 1. Phylogenetic relationships, timing of divergence events (in millions of years; MYA) and geographic distribution among human lice based on the mitochondrial COX1 gene , , .

Height of the triangles represents the number of specimens in each clade. Figure modified from .

Figure 2. Analytical pipeline used to develop microsatellite loci from genomic data including the development of multiplexes using multiple fluorescently labeled universal primers.

Ta: Annealing temperature. (see Methods S1 for details and references).

Figure 3. F _IS estimates by locus within populations.

For monomorphic loci estimates were not calculated and they are shown in the graphs as gaps. Stars indicate significant departure from Hardy-Weinberg equilibrium (P<0.05).

Figure 4. Genetic clusters inferred from STRUCTURE simulations (K = 4) for each dataset.

A) the worldwide dataset for 14 loci (we excluded M2-13 due to missing data), and B) the worldwide dataset for all 14 loci plus the mitochondrial haplogroup coded as an additional locus. In the bar plot, each individual is represented by a single vertical line and the length of each color segment represents the proportion of membership (Q) to the four clusters. In pannel B, for each louse sample we added the mitochondrial haplogroup as filled black squares for Clade A and the open diamonds representing Clade B. Distributions of points in the first two dimensions resulting from principal coordination analyses (PCA) conducted using pairwise genetic distance comparisons of the same dataset used for the STRUCTURE analyses are below each STRUCTURE plot.

Figure 5. STRUCTURE results for each geographic site with 10 or more lice: Canada, New York, Honduras and Cambodia (based on average membership coefficient, Q, derived from 14 microsatellite loci).

Figure 6. Map depicting the geographic distribution of the nuclear genetic diversity among the human louse populations included in this study.

Colored circles on map indicate collecting sites, with the color of each circle corresponding to the majority nuclear genetic cluster to which sampled individuals were assigned. Large colored circles are sites with 16 or more lice, small colored circles represent sites with one to three lice. Thick grey arrows indicate proposed migrations of anatomically modern humans out of Africa into Europe, Asia and the Americas, as well as the more recent European colonization of the New World. Colored arrows represent hypothetical human louse co-migrations. The bottom panel is the plot from STRUCTURE corresponding to the assignment of 93 lice from 11 geographical sites (from Figure 4A).