Julie M Allen

University of Illinois, Urbana-Champaign, Urbana, Illinois, United States

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Publications (16)50.64 Total impact

  • BMC Bioinformatics 12/2015; 16(1). DOI:10.1186/s12859-015-0515-2 · 2.67 Impact Factor
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    ABSTRACT: While parasitic lice (Insecta: Phthiraptera) have historically been an important model taxon for understanding host‐parasite coevolution, very few molecular markers have been developed for phylogenetic analysis. The current markers are insufficient to resolve many of the deeper nodes in this group; therefore, sequences from additional genetic loci are necessary. Here, we design primers targeting several nuclear protein coding genes based on a complete genome and transcriptome of Pediculus humanus L. plus transcriptomes and modest coverage genomic data from five genera of avian feather lice. These primers were tested on 32 genera of avian feather lice (Ischnocera), including multiple species within some genera. All of the new primer combinations produced sequences for the majority of the genera and had similar or higher divergences than the most widely used nuclear protein-coding gene in lice, EF-1α. These results indicate that these new loci will be useful in resolving phylogenetic relationships among parasitic lice.
    Journal of Medical Entomology 11/2014; 51(6). DOI:10.1603/ME13218 · 1.82 Impact Factor
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    ABSTRACT: The obligate-heritable endosymbionts of insects possess some of the smallest known bacterial genomes. This is likely due to loss of genomic material during symbiosis. The mode and rate of this erosion may change over evolutionary time; faster in newly formed associations and slower in long-established ones. The endosymbionts of human and anthropoid primate lice present a unique opportunity to study genome erosion in newly established (or young) symbionts. This is because we have a detailed phylogenetic history of these endosymbionts with divergence dates for closely related species. This allows for genome evolution to be studied in detail and rates of change to be estimated in a phylogenetic framework. Here we sequenced the genome of the chimpanzee louse endosymbiont (Candidatus Riesia pediculischaeffi) and compared it to the closely related genome of the human body louse endosymbiont. From this comparison we found evidence for recent genome erosion leading to gene loss in these endosymbionts. While gene loss was detected, it was not significantly higher than in older endosymbionts from aphids and ants. Additionally, we searched for genes associated with B-vitamin synthesis in the two louse endosymbiont genomes because these endosymbionts are believed to synthesize essential B-vitamins absent in the louse's diet. All of the expected genes were present, except those involved in thiamin synthesis. We failed to find genes encoding for proteins involved in the biosynthesis of thiamin or any exogenous means of salvaging thiamin, suggesting there is an undescribed mechanism for the salvage of thiamin. Finally, genes encoding for the pantothenate de novo biosynthesis pathway were located on a plasmid in both taxa along with a heat shock protein. Movement of these genes onto a plasmid may be functionally and evolutionarily significant, potentially increasing production and guarding against the deleterious effects of mutation. These data add to a growing resource of obligate endosymbiont genomes and to our understanding of the rate and mode of genome erosion in obligate animal-associated bacteria. Ultimately sequencing additional louse p-endosymbiont genomes will provide a model system for studying genome evolution in obligate host associated bacteria.
    G3-Genes Genomes Genetics 09/2014; DOI:10.1534/g3.114.012567 · 2.51 Impact Factor
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    ABSTRACT: There is an emerging consensus that undergraduate biology education in the United States is at a crucial juncture, especially as we acknowledge the need to train a new generation of scientists to meet looming environmental and health crises. Digital resources for biology now available online provide an opportunity to transform biology curricula to include more authentic and inquiry-driven educational experiences. Digitized natural history collections have become tremendous assets for research in environmental and health sciences, but, to date, these data remain largely untapped by educators. Natural history collections have the potential to help transform undergraduate science education from passive learning into an active exploration of the natural world, including the exploration of the complex relationships among environmental conditions, biodiversity, and human well-being. By incorporating natural history specimens and their associated data into undergraduate curricula, educators can promote participatory learning and foster an understanding of essential interactions between organisms and their environments.
    BioScience 08/2014; 64(8):725-734. DOI:10.1093/biosci/biu096 · 5.44 Impact Factor
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    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. DOI:10.1098/rspb.2013.2174 · 5.29 Impact Factor
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    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. DOI:10.1002/ece3.576 · 1.66 Impact Factor
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    ABSTRACT: Dispersal is a major life history trait of social organisms influencing the behavioral and genetic structure of their groups. Unfortunately, primate dispersal is difficult to quantify, because of the rarity of these events and our inability to ascertain if individuals dispersed or died when they disappear. Socioecological models have been partially developed to understand the ecological causes of different dispersal systems and their social consequences. However, these models have yielded confusing results when applied to folivores. The folivorous red colobus monkey (Procolobus rufomitratus) in Kibale National Park, Uganda is thought to exhibit female-biased dispersal, although both sexes have been observed to disperse and there remains considerable debate over the selective pressures favoring the transfers of males and females and the causes of variation in the proportion of each sex to leave the natal group. We circumvent this problem by using microsatellite DNA data to investigate the prediction that female dispersal will be more frequent in larger groups as compared to smaller ones. The rationale for this prediction is that red colobus exhibit increased within-group competition in bigger groups, which should favor higher female dispersal rates and ultimately lower female relatedness. Genetic data from two unequally sized neighboring groups of red colobus demonstrate increased female relatedness within the smaller group, suggesting females are less likely to disperse when there is less within-group competition. We suggest that the dispersal system is mediated to some degree by scramble competition and group size. Since red colobus group sizes have increased throughout Kibale by over 50% in the last decade, these changes may have major implications for the genetic structure and ultimately the population viability of this endangered primate. Am. J. Primatol. 00:1-13, 2013. © 2013 Wiley Periodicals, Inc.
    American Journal of Primatology 05/2013; 75(5). DOI:10.1002/ajp.22124 · 2.14 Impact Factor
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    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. DOI:10.1002/ece3.395 · 1.66 Impact Factor
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    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. DOI:10.1645/GE-3060.1 · 1.26 Impact Factor
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    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. KeywordsPodomys-Genetic diversity-Heterozygosity-Microsatellites
    Conservation Genetics Resources 01/2011; 3(1):135-139. DOI:10.1007/s12686-010-9308-0 · 1.14 Impact Factor
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    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.
    BMC Evolutionary Biology 09/2010; 10:292. DOI:10.1186/1471-2148-10-292 · 3.41 Impact Factor
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    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. DOI:10.1371/journal.pone.0004969 · 3.53 Impact Factor
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    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. DOI:10.1645/GE-1618.1 · 1.26 Impact Factor
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    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. DOI:10.1096/fj.06-6808com · 5.48 Impact Factor
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    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. DOI:10.1128/AEM.01877-06 · 3.95 Impact Factor
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    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.
    BMC Biology 02/2007; 5:7. DOI:10.1186/1741-7007-5-7 · 7.43 Impact Factor

Publication Stats

189 Citations
50.64 Total Impact Points

Institutions

  • 2014
    • University of Illinois, Urbana-Champaign
      • Illinois Natural History Survey
      Urbana, Illinois, United States
  • 2011–2013
    • University of Florida
      • Department of Biology
      Gainesville, Florida, United States
  • 2007–2012
    • Florida Museum of Natural History
      Gainesville, Florida, United States