[show abstract][hide abstract] ABSTRACT: The rate of DNA mutation and divergence is highly variable across the tree of life. However, the reasons underlying this variation are not well understood. Comparing the rates of genetic changes between hosts and parasite lineages that diverged at the same time is one way to begin to understand differences in genetic mutation and substitution rates. Such studies have indicated that the rate of genetic divergence in parasites is often faster than that of their hosts when comparing single genes. However, the variation in this relative rate of molecular evolution across different genes in the genome is unknown. We compared the rate of DNA sequence divergence between humans, chimpanzees and their ectoparasitic lice for 1534 protein-coding genes across their genomes. The rate of DNA substitution in these orthologous genes was on average 14 times faster for lice than for humans and chimpanzees. In addition, these rates were positively correlated across genes. Because this correlation only occurred for substitutions that changed the amino acid, this pattern is probably produced by similar functional constraints across the same genes in humans, chimpanzees and their ectoparasites.
Proceedings of the Royal Society B: Biological Sciences 01/2014; 281(1777):20132174. · 5.68 Impact Factor
[show abstract][hide abstract] ABSTRACT: We evaluated the mtDNA divergence and relationships within Geomys pinetis to assess the status of formerly recognized Geomys taxa. Additionally, we integrated new hypothesis-based tests in ecological niche models (ENM) to provide greater insight into causes for divergence and potential barriers to gene flow in Southeastern United States (Alabama, Florida, and Georgia). Our DNA sequence dataset confirmed and strongly supported two distinct lineages within G. pinetis occurring east and west of the ARD. Divergence date estimates showed that eastern and western lineages diverged about 1.37 Ma (1.9 Ma-830 ka). Predicted distributions from ENMs were consistent with molecular data and defined each population east and west of the ARD with little overlap. Niche identity and background similarity tests were statistically significant suggesting that ENMs from eastern and western lineages are not identical or more similar than expected based on random localities drawn from the environmental background. ENMs also support the hypothesis that the ARD represents a ribbon of unsuitable climate between more suitable areas where these populations are distributed. The estimated age of divergence between eastern and western lineages of G. pinetis suggests that the divergence was driven by climatic conditions during Pleistocene glacial-interglacial cycles. The ARD at the contact zone of eastern and western lineages of G. pinetis forms a significant barrier promoting microgeographic isolation that helps maintain ecological and genetic divergence.
Ecology and Evolution 06/2013; 3(6):1603-1613. · 1.18 Impact Factor
[show abstract][hide abstract] ABSTRACT: Red colobus monkeys, due to their sensitivity to environmental change, are indicator species of the overall health of their tropical rainforest habitats. As a result of habitat loss and overhunting, they are among the most endangered primates in the world, with very few viable populations remaining. Traditionally, extant indicator species have been used to signify the conditions of their current habitats, but they have also been employed to track past environmental conditions by detecting previous population fluctuations. Kibale National Park (KNP) in Uganda harbors the only remaining unthreatened large population of red colobus. We used microsatellite DNA to evaluate the historical demography of these red colobus and, therefore, the long-term stability of their habitat. We find that the red colobus population throughout KNP has been stable for at least ∼40,000 years. We interpret this result as evidence of long-term forest stability because a change in the available habitat or population movement would have elicited a corresponding change in population size. We conclude that the forest of what is now Kibale National Park may have served as a Late Pleistocene refuge for many East African species.
Ecology and Evolution 11/2012; 2(11):2829-42. · 1.18 Impact Factor
[show abstract][hide abstract] ABSTRACT: Abstract : Parasitic lice have been valuable informants of their host's evolutionary history because they complete their entire life cycle on the host and move between hosts primarily through direct host-to-host contact. Therefore, lice are confined to their hosts both in ecological and evolutionary time. Lice on great apes have been studied to examine details of their host's evolutionary history; however, species of Pedicinus , which parasitize the Old World monkeys, are less well known. We sampled lice from 2 groups of red colobus ( Procolobus spp.) in Kibale National Park in Uganda and from red colobus and black and white colobus ( Procolobus polycomos ) in Taï National Park in Côte d'Ivoire. We used next-generation sequencing data analysis and the human body louse ( Pediculus humanus humanus ) genome to search for microsatellites for population genetic studies of Pedicinus lice. The 96 primer sets for microsatellite loci designed from the human body louse genome failed to amplify microsatellites in Pedicinus sp., perhaps due to the fast rate of evolution in parasitic lice. Of 63 microsatellites identified by next-generation sequencing data analysis of Pedicinus sp., 12 were variable among populations and 9 were variable within a single population. Our results suggest that these loci will be useful across the genus Pedicinus . We found that the lice in Uganda are not structured according to their hosts' social group; rather, 2 non-interbreeding populations of lice were found on both groups of red colobus. Because direct host-to-host contact is usually required for lice to move among hosts, these lice could be useful for identification and study of behavioral interactions between primate species.
Journal of Parasitology 04/2012; 98(5):930-7. · 1.32 Impact Factor
[show abstract][hide abstract] ABSTRACT: The Florida mouse (Podomys floridanus) is endemic to Florida and is considered vulnerable by the IUCN due to extensive habitat loss. Here, we describe a panel of 76 microsatellite DNA markers for population genetic
studies of this species. Fourteen of these loci were examined to estimate genetic diversity for 39 specimens collected in
Florida in 1957 and 2006. DNA extractions from the 1957 specimens were carried out from snips of skin taken from museum voucher
skins, whereas the 2006 samples were extracted from fresh liver tissue. The use of museum skins for reconstructing the genetics
of historical populations is becoming a critical part of understanding past, present, and future genetic trends for threatened
species. Mean expected heterozygosity for the two populations was 0.73 and mean observed heterozygosity was 0.75. The number
of alleles per locus ranged from 2 to 15. All microsatellites were polymorphic, and exhibited variability across time.
[show abstract][hide abstract] ABSTRACT: 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.
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.
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.
[show abstract][hide abstract] ABSTRACT: Primary bacterial endosymbionts of insects (p-endosymbionts) are thought to be undergoing the process of Muller's ratchet where they accrue slightly deleterious mutations due to genetic drift in small populations with negligible recombination rates. If this process were to go unchecked over time, theory predicts mutational meltdown and eventual extinction. Although genome degradation is common among p-endosymbionts, we do not observe widespread p-endosymbiont extinction, suggesting that Muller's ratchet may be slowed or even stopped over time. For example, selection may act to slow the effects of Muller's ratchet by removing slightly deleterious mutations before they go to fixation thereby causing a decrease in nucleotide substitutions rates in older p-endosymbiont lineages.
To determine whether selection is slowing the effects of Muller's ratchet, we determined the age of the Candidatus Riesia/sucking louse assemblage and analyzed the nucleotide substitution rates of several p-endosymbiont lineages that differ in the length of time that they have been associated with their insect hosts. We find that Riesia is the youngest p-endosymbiont known to date, and has been associated with its louse hosts for only 13-25 My. Further, it is the fastest evolving p-endosymbiont with substitution rates of 19-34% per 50 My. When comparing Riesia to other insect p-endosymbionts, we find that nucleotide substitution rates decrease dramatically as the age of endosymbiosis increases.
A decrease in nucleotide substitution rates over time suggests that selection may be limiting the effects of Muller's ratchet by removing individuals with the highest mutational loads and decreasing the rate at which new mutations become fixed. This countering effect of selection could slow the overall rate of endosymbiont extinction.
PLoS ONE 02/2009; 4(3):e4969. · 3.73 Impact Factor
[show abstract][hide abstract] ABSTRACT: Human head lice (Pediculus humanus capitis) are subdivided into 3 deeply divergent mitochondrial clades (Clades A, B, and C), each having unique geographical distributions. Determining the evolutionary history and geographic distribution of these mitochondrial clades can elucidate the evolutionary history of the lice as well as their human hosts. Previous data suggest that lice belonging to mitochondrial Clade B may have originated in North America or Asia; however, geographic sampling and sample sizes have been limited. With newly collected lice, we calculate the relative frequency, geographic distribution, and genetic diversity of louse mitochondrial clades to determine the geographic origin of lice belonging to Clade B. In agreement with previous studies, genetic diversity data support a North American origin of Clade B lice. It is likely that lice belonging to this mitochondrial clade recently migrated to other geographic localities, e.g., Europe and Australia, and, if not already present, may disperse further to occupy all geographic regions.
Journal of Parasitology 06/2008; 94(6):1275-81. · 1.32 Impact Factor
[show abstract][hide abstract] ABSTRACT: The first mycetome was discovered more than 340 yr ago in the human louse. Despite the remarkable biology and medical and social importance of human lice, its primary endosymbiont has eluded identification and characterization. Here, we report the host-symbiont interaction of the mycetomic bacterium of the head louse Pediculus humanus capitis and the body louse P. h. humanus. The endosymbiont represents a new bacterial lineage in the gamma-Proteobacteria. Its closest sequenced relative is Arsenophonus nasoniae, from which it differs by more than 10%. A. nasoniae is a male-killing endosymbiont of jewel wasps. Using microdissection and multiphoton confocal microscopy, we show the remarkable interaction of this bacterium with its host. This endosymbiont is unique because it occupies sequentially four different mycetomes during the development of its host, undergoes three cycles of proliferation, changes in length from 2-4 microm to more than 100 microm, and has two extracellular migrations, during one of which the endosymbionts have to outrun its host's immune cells. The host and its symbiont have evolved one of the most complex interactions: two provisional or transitory mycetomes, a main mycetome and a paired filial mycetome. Despite the close relatedness of body and head lice, differences are present in the mycetomic provisioning and the immunological response.
The FASEB Journal 05/2007; 21(4):1058-66. · 5.70 Impact Factor
[show abstract][hide abstract] ABSTRACT: The primary endosymbiotic bacteria from three species of parasitic primate lice were characterized molecularly. We have confirmed the characterization of the primary endosymbiont (P-endosymbiont) of the human head/body louse Pediculus humanus and provide new characterizations of the P-endosymbionts from Pediculus schaeffi from chimpanzees and Pthirus pubis, the pubic louse of humans. The endosymbionts show an average percent sequence divergence of 11 to 15% from the most closely related known bacterium "Candidatus Arsenophonus insecticola." We propose that two additional species be added to the genus "Candidatus Riesia." The new species proposed within "Candidatus Riesia" have sequence divergences of 3.4% and 10 to 12% based on uncorrected pairwise differences. Our Bayesian analysis shows that the branching pattern for the primary endosymbionts was the same as that for their louse hosts, suggesting a long coevolutionary history between primate lice and their primary endosymbionts. We used a calibration of 5.6 million years to date the divergence between endosymbionts from human and chimpanzee lice and estimated an evolutionary rate of nucleotide substitution of 0.67% per million years, which is 15 to 30 times faster than previous estimates calculated for Buchnera, the primary endosymbiont in aphids. Given the evidence for cospeciation with primate lice and the evidence for fast evolutionary rates, this lineage of endosymbiotic bacteria can be evaluated as a fast-evolving marker of both louse and primate evolutionary histories.
Applied and Environmental Microbiology 04/2007; 73(5):1659-64. · 3.68 Impact Factor
[show abstract][hide abstract] ABSTRACT: 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.
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.
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.