Evolutionary history of mammalian sucking lice (Phthiraptera: Anoplura)

Abstract

Background: Sucking lice (Phthiraptera: Anoplura) are obligate, permanent ectoparasites of eutherian mammals, parasitizing members of 12 of the 29 recognized mammalian orders and approximately 20% of all mammalian species. These host specific, blood-sucking insects are morphologically adapted for life on mammals: they are wingless, dorso-ventrally flattened, possess tibio-tarsal claws for clinging to host hair, and have piercing mouthparts for feeding. Although there are more than 540 described species of Anoplura and despite the potential economical and medical implications of sucking louse infestations, this study represents the first attempt to examine higher-level anopluran relationships using molecular data. In this study, we use molecular data to reconstruct the evolutionary history of 65 sucking louse taxa with phylogenetic analyses and compare the results to findings based on morphological data. We also estimate divergence times among anopluran taxa and compare our results to host (mammal) relationships.

Results: This study represents the first phylogenetic hypothesis of sucking louse relationships using molecular data and we find significant conflict between phylogenies constructed using molecular and morphological data. We also find that multiple families and genera of sucking lice are not monophyletic and that extensive taxonomic revision will be necessary for this group. Based on our divergence dating analyses, sucking lice diversified in the late Cretaceous, approximately 77 Ma, and soon after the Cretaceous-Paleogene boundary (ca. 65 Ma) these lice proliferated rapidly to parasitize multiple mammalian orders and families.

Conclusions: The diversification time of sucking lice approximately 77 Ma is in agreement with mammalian evolutionary history: all modern mammal orders are hypothesized to have diverged by 75 Ma thus providing suitable habitat for the colonization and radiation of sucking lice. Despite the concordant timing of diversification events early in the association between anoplurans and mammals, there is substantial conflict between the host and parasite phylogenies. This conflict is likely the result of a complex history of host switching and extinction events that occurred throughout the evolutionary association between sucking lice and their mammalian hosts. It is unlikely that there are any ectoparasite groups (including lice) that tracked the early and rapid radiation of eutherian mammals.

Figure 1

Hypothesized relationships among Anoplura families (and their host associations) redrawn from Kim [22].

Figure 2

Bayesian phylogram of the Anoplura based on molecular data. This Bayesian phylogram is the result from the analysis of the combined 3-gene data set partitioning the data by gene and by codon for the protein coding genes COI and EF-1α. Bayesian posterior probability greater than 0.95 and likelihood support values greater than 75 are indicated by the heavy branches. Taxon names correspond to Additional File 1 and taxon colors correspond to louse family. Louse family and host associations are indicated to the right of each clade. A monophyletic Anoplura is indicated by the arrow.

Figure 3

Chronogram for the Anoplura. Shown is the Bayesian topology resulting from analysis of the 3-gene data set (partitioning the data by gene and by codon for the protein coding genes COI and EF-1α) in BEAST [36], which differs only slightly from the topology shown in Figure 2 (there is weak support for these differences; see text). Divergence times were estimated using three calibrations (94-101 Ma for the spilt between Rhynchophthirina and Anoplura, 20-25 Ma for the split between Old World Monkey lice and hominoid lice, and 5-7 Ma for the split between human and chimpanzee-associated Pediculus lice), indicated by filled circles at nodes. Taxon colors correspond to louse family indicated in Figure 2 and host associations are indicated to the right of each clade. The Cretaceous-Paleogene (K-Pg) boundary is indicated at 65 Ma by the dark gray vertical bar. Upper and lower bounds of the 95% highest posterior density interval (95% HPD) for each node are available in Additional File 5.

Figure 4

Comparison of host and parasite chronograms. The parasite chronogram is redrawn from Figure 3 and the host chronogram (with dates of major mammalian divergences) is redrawn from Bininda-Emonds et al. [20]. Lines drawn between taxa indicate host-parasite associations. On the host chronogram, lineages with red and yellow boxes are parasitized by sucking lice and chewing lice, respectively. Mammalian lineages without shaded boxes are not known to be parasitized by any louse group. The Cretaceous-Paleogene (K-Pg) boundary indicated at 65 Ma by the dark gray vertical bar.