Evolutionary history of mammalian sucking lice (Phthiraptera: Anoplura)

Abstract

BackgroundSucking 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.ResultsThis 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.ConclusionsThe 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.

Multiple lineages of lice pass through the K–Pg boundary

“…BEAST analysis recovers a chronogram for lice (figure 1) that is consistent with recent studies of phthirapteran phylogeny [12,19]. The monophyly of each louse suborder is generally well-supported and the psocopteran Liposcelis is sister taxon to the Amblycera, supporting the polyphyly of Phthiraptera [20].…”

“…The timing of the diversification of sucking lice in the Late Cretaceous (approx. 75 Ma) and subsequent radiation soon after the K-Pg boundary is in agreement with mammalian evolutionary history [7] and a recent study focused solely on the Anoplura [19]. Interestingly, the diversification of extant chewing lice parasitizing mammals postdates the K -Pg boundary, in contrast to the Cretaceous diversification of their avian infesting relatives.…”

Anoplurans (Insecta: Psocodea: Anoplura) associated with rodents distributed in the neotropical region of Mexico

“…The sequences obtained were submitted to GenBank. Additionally to our sequences, we obtained another 25 from GenBank belonging to the families Hoplopleuridae and Polyplacidae, and 1 Ischnoceran (Columbicola columbae), which was used as an outgroup in accordance with the proposal of Light et al (2010), with the following accession numbers: AF385003, AF545717, DQ324548, DQ324549, DQ324564, DQ324578, EU162163, EU375771, HM171425, HM171426, HM171427, HM171428, HM171429, HM171430, HM171431, HM171432, HM171433, HM171442, HM171443, HM171444, HM171445, HQ542195, HQ542196.…”

“…Currently, 550 species of Anoplura distributed in 16 families and 49 genera have been recorded worldwide (Durden & Musser, 1994;Light, Smith, Allen, Durden, & Reed, 2010); two-thirds of these arthropods belong to the families Polyplacidae and Hoplopleuridae, both including species parasites of rodents (Durden, 2002). The inventory of Mexican sucking lice is conformed by 44 species distributed in 8 genera (Antarctophthirus Enderlein, 1906;Enderleinellus Fahrenholz, 1912;Fahrenholzia Kellogg and Ferris, 1919;Hoplopleura Enderlein, 1904;Linognathoides Cummings, 1914;Linognathus Enderlein, 1905;Neohaematopinus Mjöberg, 1910 andPolyplax Enderlein, 1904) and 5 families (Echinophthiriidae, Enderleinellidae, Hoplopleuridae, Linognathidae and Polyplacidae).…”

Novel Primers From Informative Nuclear Loci for Louse Molecular Phylogenetics (Insecta: Phthiraptera)

“…Despite their importance as a model organism in hostÐparasite studies, very few loci have been targeted for sequencing in parasitic lice. A large number of studies have been published on the molecular phylogenetics of parasitic lice (Hafner et al 1994;Page et al 1998Page et al , 2004Cruickshank et al 2001;Johnson et al 2001aJohnson et al ,b, 2002aJohnson et al ,b, 2003Johnson et al , 2007Weckstein 2004;Banks et al 2005;Light and Hafner 2008;Š tefka and Hypsa 2008;Bueter et al 2009;Light et al 2010;Š tefka et al 2011), but most of these studies have only used short fragments of the mitochondrial cytochrome oxidase subunit-1 (CO1) and nuclear elongation factor-1 alpha (EF-1␣) for phylogenetic analysis. The generally small amount of data in these studies makes resolving many of the branches in the phylogenetic tree difÞcult.…”