Genetic analysis of lice supports direct contact between modern and archaic humans

Abstract

Parasites can be used as unique markers to investigate host evolutionary history, independent of host data. Here we show that modern human head lice, Pediculus humanus, are composed of two ancient lineages, whose origin predates modern Homo sapiens by an order of magnitude (ca. 1.18 million years). One of the two louse lineages has a worldwide distribution and appears to have undergone a population bottleneck ca. 100,000 years ago along with its modern H. sapiens host. Phylogenetic and population genetic data suggest that the other lineage, found only in the New World, has remained isolated from the worldwide lineage for the last 1.18 million years. The ancient divergence between these two lice is contemporaneous with splits among early species of Homo, and cospeciation analyses suggest that the two louse lineages codiverged with a now extinct species of Homo and the lineage leading to modern H. sapiens. If these lice indeed codiverged with their hosts ca. 1.18 million years ago, then a recent host switch from an archaic species of Homo to modern H. sapiens is required to explain the occurrence of both lineages on modern H. sapiens. Such a host switch would require direct physical contact between modern and archaic forms of Homo.

Figure 1. Phylogeny of Primate Lice from Morphological and Molecular Data

The phylogeny is a strict consensus of morphology and a 1,525-bp fragment of COI and Cytb. Branch lengths were determined from the molecular data. Numbers in parentheses are bootstrap values from molecular and morphological data, respectively. Divergence dates are direct estimates from mtDNA data (see text). Louse images from light microscopy were taken by VSS.

Figure 2. Molecular Phylogeny of P. humanus from Geographically Diverse Human Populations

This species exhibits distinct “head” and “body” forms, which differ in ecology, and slightly in size. Head lice (black lettering) are smaller than body lice (red lettering) and are confined to the scalp, whereas body lice live primarily in clothing. Haplotypes shown in green were found in both head and body lice. There are no fixed genetic differences between the head and body forms, suggesting a lack of reproductive isolation, despite the fact that the two forms can be distinguished using discriminant function analysis of morphological data. These results are consistent with experimental data showing that head lice can transform morphologically into body lice within a few generations (Levene and Dobzhansky 1959). The Worldwide clade (red branches) shares a MRCA ca. 0.54 MYA and the geographically restricted New World clade (blue branches) has a much younger MRCA, ca. 0.15 MYA. Asterisks denote samples from Leo et al. (2002)

Figure 3. Plot of the First and Second Canonical Discriminant Functions for Specimens of Adult Head/Body Lice (P. humanus) and Pubic Lice (Pthirus pubis)

Solid points denote reference specimens of known identity acquired from museum collections. Unfilled points denote newly collected specimens used in the molecular analyses. In all cases the discriminant function analysis successfully classified each unknown case with a probability of >0.95.

Figure 4. Neighbor-Joining Tree Using a Best-Fit Model of Nucleotide Substitution (Tamura-Nei + Γ) for a Combined Data Set of Cytb Sequences from Our Study and from Kittler et al. (2003)

The clades of P. humanus identified by Kittler et al. (2003) are nearly identical to those from our data, with the exception of their basal African clade, which was not represented in our data set. One clade contains both head lice and body lice and is WW in distribution. Another clade is comprised solely of head lice from the NW (our data) and Europe (samples from Kittler et al. 2003), and the most basal clade contains isolates 4, 18, and 33 from Kittler et al. (2003), which are head lice from Africa. The size of the triangles representing the three clades are proportional in size to the number of taxa within the clade. This phylogeny is rooted with a divergent louse, Dennyus hirundinus, which is a bird louse in the suborder Amblycera. Note the placement of the Kittler et al. (2003) specimen of P. schaeffi, which falls outside all other primate lice and the rodent louse Fahrenholzia.

Figure 5. Temporal and Geographical Distribution of Hominid Populations Redrawn from Stringer (2003)

This figure depicts one view of human evolutionary history based on fossil data. Other interpretations differ primarily in the taxonomy and geographical distribution of hominid species. The temporal distribution of the two divergent lineages of P. humanus is superimposed on the hominid tree to show host evolutionary events that were contemporaneous with the origin of P. humanus. Whereas the NW lineage is depicted on H. erectus in this figure, several alternative hypotheses are consistent with our data when other evolutionary histories of hominids are considered (unpublished data). The WW clade is shown in red and the NW clade in blue (see text for descriptions of clades).