Nuclear genetic diversity of head lice sheds light on human dispersal around the world

The human louse, Pediculus humanus, is an obligate blood-sucking ectoparasite that has coevolved with humans for millennia. Given the intimate relationship between this parasite and the human host, the study of human lice has the potential to shed light on aspects of human evolution that are difficult to interpret using other biological evidence. In this study, we analyzed the genetic variation in 274 human lice from 25 geographic sites around the world by using nuclear microsatellite loci and female-inherited mitochondrial DNA sequences. Nuclear genetic diversity analysis revealed the presence of two distinct genetic clusters I and II, which are subdivided into subclusters: Ia-Ib and IIa-IIb, respectively. Among these samples, we observed the presence of the two most common louse mitochondrial haplogroups: A and B that were found in both nuclear Clusters I and II. Evidence of nuclear admixture was uncommon (12%) and was predominate in the New World potentially mirroring the history of colonization in the Americas. These findings were supported by novel DIYABC simulations that were built using both host and parasite data to define parameters and models suggesting that admixture between cI and cII was very recent. This pattern could also be the result of a reproductive barrier between these two nuclear genetic clusters. In addition to providing new evolutionary knowledge about this human parasite, our study could guide the development of new analyses in other host-parasite systems.

[1]  R. Shao,et al.  Fragmented mitochondrial genomes of seal lice (family Echinophthiriidae) and gorilla louse (family Pthiridae): frequent minichromosomal splits and a host switch of lice between seals , 2022, BMC Genomics.

[2]  J. V. Moreno-Mayar,et al.  Ancient Human Genomes and Environmental DNA from the Cement Attaching 2,000-Year-Old Head Lice Nits , 2021, Molecular biology and evolution.

[3]  S. Payungporn,et al.  Molecular analysis of mitochrondrial cytb of Pediculus humanus capitis in Thailand revealed potential historical connection with South Asia , 2021, PloS one.

[4]  B. Oldroyd,et al.  How does epigenetics influence the course of evolution? , 2021, Philosophical Transactions of the Royal Society B.

[5]  B. Oldroyd,et al.  The role of epigenetics, particularly DNA methylation, in the evolution of caste in insect societies , 2021, Philosophical Transactions of the Royal Society B.

[6]  R. Pollack,et al.  International recommendations for an effective control of head louse infestations , 2020, International journal of dermatology.

[7]  M. Miyamoto,et al.  A Fly on the Cave Wall: Parasite Genetics Reveal Fine-scale Dispersal Patterns of Bats. , 2019, The Journal of parasitology.

[8]  M. Ashfaq,et al.  Mitochondrial diversity and phylogeographic analysis of Pediculus humanus reveals a new Amazonian clade "F". , 2019, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[9]  M. Shunkov,et al.  Age estimates for hominin fossils and the onset of the Upper Palaeolithic at Denisova Cave , 2019, Nature.

[10]  Laguna,et al.  About Head Lice Transmission From Field Data and Mathematical Modeling , 2019 .

[11]  J. Clark,et al.  The unusual reproductive system of head and body lice (Pediculus humanus) , 2017, Medical and veterinary entomology.

[12]  S. Pääbo,et al.  Direct dating of Neanderthal remains from the site of Vindija Cave and implications for the Middle to Upper Paleolithic transition , 2017, Proceedings of the National Academy of Sciences.

[13]  Julie M. Allen,et al.  Primates, Lice and Bacteria: Speciation and Genome Evolution in the Symbionts of Hominid Lice , 2017, Molecular biology and evolution.

[14]  Mattias Jakobsson,et al.  Tracing the peopling of the world through genomics , 2017, Nature.

[15]  D. Raoult,et al.  High Ancient Genetic Diversity of Human Lice, Pediculus humanus, from Israel Reveals New Insights into the Origin of Clade B Lice , 2016, PloS one.

[16]  D. Raoult,et al.  Human Lice in Paleoentomology and Paleomicrobiology. , 2016, Microbiology spectrum.

[17]  S. Blanchet,et al.  Host dispersal as the driver of parasite genetic structure: a paradigm lost? , 2016, Ecology letters.

[18]  Ilan Gronau,et al.  Ancient gene flow from early modern humans into Eastern Neanderthals , 2016, Nature.

[19]  D. Raoult,et al.  A New Clade of African Body and Head Lice Infected by Bartonella quintana and Yersinia pestis-Democratic Republic of the Congo. , 2015, The American journal of tropical medicine and hygiene.

[20]  A. Moya,et al.  Solving a Bloody Mess: B-Vitamin Independent Metabolic Convergence among Gammaproteobacterial Obligate Endosymbionts from Blood-Feeding Arthropods and the Leech Haementeria officinalis , 2015, Genome biology and evolution.

[21]  M. Ashfaq,et al.  High diversity and rapid diversification in the head louse, Pediculus humanus (Pediculidae: Phthiraptera) , 2015, Scientific Reports.

[22]  Mattias Jakobsson,et al.  Genomic evidence for the Pleistocene and recent population history of Native Americans , 2015, Science.

[23]  G. Kerth,et al.  Host and parasite life history interplay to yield divergent population genetic structures in two ectoparasites living on the same bat species , 2015, Molecular ecology.

[24]  T. Pengsakul,et al.  Molecular survey of the head louse Pediculus humanus capitis in Thailand and its potential role for transmitting Acinetobacter spp. , 2015, Parasites & Vectors.

[25]  G. Perry.  Parasites and human evolution , 2014, Evolutionary anthropology.

[26]  E. Carbonell,et al.  Neandertal roots: Cranial and chronological evidence from Sima de los Huesos , 2014, Science.

[27]  Jean-Marie Cornuet,et al.  DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data , 2014, Bioinform..

[28]  Julie M. Allen,et al.  Rates of genomic divergence in humans, chimpanzees and their lice , 2014, Proceedings of the Royal Society B: Biological Sciences.

[29]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[30]  D. Reed,et al.  Mitochondrial diversity in human head louse populations across the Americas. , 2013, American journal of physical anthropology.

[31]  R. DeSalle,et al.  Lack of population genetic structure and host specificity in the bat fly, Cyclopodia horsfieldi, across species of Pteropus bats in Southeast Asia , 2013, Parasites & Vectors.

[32]  August E. Woerner,et al.  Higher Levels of Neanderthal Ancestry in East Asians than in Europeans , 2013, Genetics.

[33]  D. Reed,et al.  Nuclear Genetic Diversity in Human Lice (Pediculus humanus) Reveals Continental Differences and High Inbreeding among Worldwide Populations , 2013, PloS one.

[34]  R. Moritz,et al.  Patterns of Evolutionary Conservation of Microsatellites (SSRs) Suggest a Faster Rate of Genome Evolution in Hymenoptera Than in Diptera , 2013, Genome biology and evolution.

[35]  Adrian W. Briggs,et al.  A High-Coverage Genome Sequence from an Archaic Denisovan Individual , 2012, Science.

[36]  R. Shao,et al.  Evolution of Extensively Fragmented Mitochondrial Genomes in the Lice of Humans , 2012, Genome biology and evolution.

[37]  Rod Peakall,et al.  GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update , 2012, Bioinform..

[38]  Carina M. Schlebusch,et al.  Age of the Association between Helicobacter pylori and Man , 2012, PLoS pathogens.

[39]  Péter Apari,et al.  Why infest the loved ones – inherent human behaviour indicates former mutualism with head lice , 2012, Parasitology.

[40]  B. vonHoldt,et al.  STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method , 2012, Conservation Genetics Resources.

[41]  E. Hoberg,et al.  Return to Beringia: parasites reveal cryptic biogeographic history of North American pikas , 2012, Proceedings of the Royal Society B: Biological Sciences.

[42]  C. Stringer,et al.  The earliest evidence for anatomically modern humans in northwestern Europe , 2011, Nature.

[43]  Stefano Benazzi,et al.  Early dispersal of modern humans in Europe and implications for Neanderthal behaviour , 2011, Nature.

[44]  J. Light,et al.  Origin of Clothing Lice Indicates Early Clothing Use by Anatomically Modern Humans in Africa , 2010, Molecular biology and evolution.

[45]  F. Balloux,et al.  Discriminant analysis of principal components: a new method for the analysis of genetically structured populations , 2010, BMC Genetics.

[46]  Jean-Marie Cornuet,et al.  Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0) , 2010, BMC Bioinformatics.

[47]  R. Ricklefs,et al.  A Molecular Clock for Malaria Parasites , 2010, Science.

[48]  G. Bertorelle,et al.  ABC as a flexible framework to estimate demography over space and time: some cons, many pros , 2010, Molecular ecology.

[49]  K. Yoshizawa,et al.  How stable is the "Polyphyly of Lice" hypothesis (Insecta: Psocodea)?: a comparison of phylogenetic signal in multiple genes. , 2010, Molecular phylogenetics and evolution.

[50]  L. Excoffier,et al.  Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows , 2010, Molecular ecology resources.

[51]  Peter Beerli,et al.  Unified Framework to Evaluate Panmixia and Migration Direction Among Multiple Sampling Locations , 2010, Genetics.

[52]  A. Moya,et al.  Evolutionary Convergence and Nitrogen Metabolism in Blattabacterium strain Bge, Primary Endosymbiont of the Cockroach Blattella germanica , 2009, PLoS genetics.

[53]  D. Graham,et al.  The Peopling of the Pacific from a Bacterial Perspective , 2009, Science.

[54]  J. Werren,et al.  Wolbachia: master manipulators of invertebrate biology , 2008, Nature Reviews Microbiology.

[55]  Noah A. Rosenberg,et al.  ADZE: a rarefaction approach for counting alleles private to combinations of populations , 2008, Bioinform..

[56]  Thibaut Jombart,et al.  adegenet: a R package for the multivariate analysis of genetic markers , 2008, Bioinform..

[57]  J. Light,et al.  What's in a name: the taxonomic status of human head and body lice. , 2008, Molecular phylogenetics and evolution.

[58]  K. Reinhard,et al.  Parasites as probes for prehistoric human migrations? , 2008, Trends in parasitology.

[59]  D. Raoult,et al.  Molecular identification of lice from pre-Columbian mummies. , 2008, The Journal of infectious diseases.

[60]  K. Mumcuoglu.  Human lice: Pediculus and Pthirus , 2008 .

[61]  H. Burbano,et al.  The Derived FOXP2 Variant of Modern Humans Was Shared with Neandertals , 2007, Current Biology.

[62]  P. Parker,et al.  Co‐phylogeography and comparative population genetics of the threatened Galápagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities , 2007, Molecular ecology.

[63]  J. Dipierri,et al.  Beringian Standstill and Spread of Native American Founders , 2007, PloS one.

[64]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[65]  Julie M. Allen,et al.  Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice , 2007, BMC Biology.

[66]  T. Fukatsu,et al.  Symbiotic Bacteria Associated with Stomach Discs of Human Lice , 2006, Applied and Environmental Microbiology.

[67]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[68]  S. Barker,et al.  Transmission ratio distortion in the human body louse, Pediculus humanus (Insecta: Phthiraptera) , 2006, Heredity.

[69]  S. Barker,et al.  Supergroup F Wolbachia bacteria parasitise lice (Insecta: Phthiraptera) , 2006, Parasitology Research.

[70]  C. Stringer,et al.  U-series and ESR analyses of bones and teeth relating to the human burials from Skhul. , 2005, Journal of human evolution.

[71]  C. Finlayson,et al.  Biogeography and evolution of the genus Homo. , 2005, Trends in ecology & evolution.

[72]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[73]  J. Fleagle,et al.  Stratigraphic placement and age of modern humans from Kibish, Ethiopia , 2005, Nature.

[74]  D. Colwell,et al.  On the ubiquity and phylogeny of Wolbachia in lice , 2004, Molecular ecology.

[75]  J. Edman,et al.  Transmission potential of the human head louse, Pediculus capitis (Anoplura: Pediculidae) , 2004, International journal of dermatology.

[76]  A. Rogers,et al.  Genetic Analysis of Lice Supports Direct Contact between Modern and Archaic Humans , 2004, PLoS biology.

[77]  M. Zelazowska,et al.  The sex ratio distortion in the human head louse is conserved over time , 2004, BMC Genetics.

[78]  O. Pybus,et al.  Unifying the Epidemiological and Evolutionary Dynamics of Pathogens , 2004, Science.

[79]  N. Rosenberg.  distruct: a program for the graphical display of population structure , 2003 .

[80]  B. Normark.  The evolution of alternative genetic systems in insects. , 2003, Annual review of entomology.

[81]  J. Edman,et al.  In Vivo and In Vitro Rearing of Pediculus humanus capitis (Anoplura: Pediculidae) , 2003, Journal of medical entomology.

[82]  M. Stoneking,et al.  Molecular Evolution of Pediculus humanus and the Origin of Clothing , 2003, Current Biology.

[83]  M. Stephens,et al.  Traces of Human Migrations in Helicobacter pylori Populations , 2003, Science.

[84]  J. Nozáis.  The origin and dispersion of human parasitic diseases in the old world (Africa, Europe and Madagascar). , 2003, Memorias do Instituto Oswaldo Cruz.

[85]  M. Blaser,et al.  East Asian genotypes of Helicobacter pylori strains in Amerindians provide evidence for its ancient human carriage , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[86]  Peter Beerli,et al.  Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[87]  C. Schlötterer.  Evolutionary dynamics of microsatellite DNA , 2000, Chromosoma.

[88]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[89]  M. Tristem.  Molecular Evolution — A Phylogenetic Approach. , 2000, Heredity.

[90]  J. Boore.  Animal mitochondrial genomes. , 1999, Nucleic acids research.

[91]  K. Wetterstrand,et al.  The mutation rates of di-, tri- and tetranucleotide repeats in Drosophila melanogaster. , 1998, Molecular biology and evolution.

[92]  R. Petit,et al.  Identifying Populations for Conservation on the Basis of Genetic Markers , 1998 .

[93]  N. Gratz.  Human lice. Their prevalence, control and resistance to insecticides. A review 1985-1997 , 1997 .

[94]  S. Nadler,et al.  Disparate rates of molecular evolution in cospeciating hosts and parasites. , 1994, Science.

[95]  R. Sukernik,et al.  mtDNA variation of aboriginal Siberians reveals distinct genetic affinities with Native Americans. , 1993, American journal of human genetics.

[96]  S. Nadler,et al.  Phylogenetic trees support the coevolution of parasites and their hosts , 1988, Nature.

[97]  N. Saito.  The neighbor-joining method : A new method for reconstructing phylogenetic trees , 1987 .

[98]  D. McLean,et al.  Observation of symbiote migration in human body lice with scanning and transmission electron microscopy. , 1983, Canadian journal of microbiology.

[99]  S. Hurlbert.  The Nonconcept of Species Diversity: A Critique and Alternative Parameters. , 1971, Ecology.

[100]  P. Buchner.  Endosymbiosis of Animals with Plant Microorganisms , 1965 .

[101]  A. Dickson.  On Evolution , 1884, Science.

[102]  J. Bullen.  Host—Parasite Relationships , 1958, Nature.

[103]  W. Kruskal,et al.  Use of Ranks in One-Criterion Variance Analysis , 1952 .

[104]  A. D. Imms.  The Louse , 1940, Nature.

[105]  G. Nuttall.  The Biology of Pediculus humanus , 1917, Parasitology.