Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice

Abstract

Background: The parasitic sucking lice of primates are known to have undergone at least 25 million years of coevolution with their hosts. For example, chimpanzee lice and human head/body lice last shared a common ancestor roughly six million years ago, a divergence that is contemporaneous with their hosts. In an assemblage where lice are often highly host specific, humans host two different genera of lice, one that is shared with chimpanzees and another that is shared with gorillas. In this study, we reconstruct the evolutionary history of primate lice and infer the historical events that explain the current distribution of these lice on their primate hosts.

Results: Phylogenetic and cophylogenetic analyses suggest that the louse genera Pediculus and Pthirus are each monophyletic, and are sister taxa to one another. The age of the most recent common ancestor of the two Pediculus species studied matches the age predicted by host divergence (ca. 6 million years), whereas the age of the ancestor of Pthirus does not. The two species of Pthirus (Pthirus gorillae and Pthirus pubis) last shared a common ancestor ca. 3-4 million years ago, which is considerably younger than the divergence between their hosts (gorillas and humans, respectively), of approximately 7 million years ago.

Conclusion: Reconciliation analysis determines that there are two alternative explanations that account for the current distribution of anthropoid primate lice. The more parsimonious of the two solutions suggests that a Pthirus species switched from gorillas to humans. This analysis assumes that the divergence between Pediculus and Pthirus was contemporaneous with the split (i.e., a node of cospeciation) between gorillas and the lineage leading to chimpanzees and humans. Divergence date estimates, however, show that the nodes in the host and parasite trees are not contemporaneous. Rather, the shared coevolutionary history of the anthropoid primates and their lice contains a mixture of evolutionary events including cospeciation, parasite duplication, parasite extinction, and host switching. Based on these data, the coevolutionary history of primates and their lice has been anything but parsimonious.

Figure 1

Phylogenetic trees for primate lice and their vertebrate hosts redrawn from Reed et al. [9]. Trees are shown as cladograms with no branch length information, and are based on molecular and morphological data. Dashed lines between trees represent host-parasite associations. Humans are unique in being parasitized by two genera (Pediculus and Pthirus). Photo credits: J. W. Demastes, T. Choe, and V. Smith.

Figure 2

Cophylogenetic reconstructions with the host phylogeny for humans, chimpanzees, gorillas, and Old World monkeys indicated by thick grey lines, and the louse phylogeny indicated by thin red and blue lines. (A) Reconstruction showing perfect cospeciation between with hosts and parasites with the exception of a single host switch of Pthirus sp. from gorillas to humans (marked by an arrow). (B) Cophylogenetic reconstruction showing an ancient duplication creating two evolutionarily distinct lineages (Pediculus and Pthirus), each having cospeciated with gorillas, chimps, and humans with two extinction events (marked with daggers). The reconciliation shown in panel A requires one evolutionary step (the host switch), whereas reconciliation B requires three steps (one duplication and two extinctions).

Figure 3

Maximum likelihood (ML) phylogeny of primate lice using the combined Cox1 and EF-1α dataset with a best-fit ML model of nucleotide substitution (left). Bootstrap values are indicated below the nodes and divergence estimates are given above. Clade numbers used in Table 1 are provided to the right of each node. The ML phylogeny of the Cox1 gene from host taxa is indicated on the right. Branch lengths are drawn to the same scale (substitutions/site), and are based on the best-fit ML model of nucleotide substitution. Dashed lines connect hosts and their associated parasites.

Figure 4

Coevolutionary reconstruction of primate lice and their hosts based on reconciliation analysis and divergence date estimation. Thick grey lines represent the host phylogeny for humans, chimpanzees, gorillas, and Old World monkeys. Thin black lines (solid and dashed) represent the louse lineages. This evolutionary scenario depicts a parasite duplication ca. 13 MYA leading to the extant genera Pediculus (solid lines) and Pthirus (dashed lines). One species from each lineage is depicted as having gone extinct (dagger), and a single host switch ca. 3–4 MYA is shown by an arrow within the Pthirus lineage. The divergence of the chimpanzee and human lice (Pediculus spp.) are shown as having diverged in tandem with their hosts.