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Research Article

Global divergence of the human follicle mite Demodex folliculorum: Persistent associations between host ancestry and mite lineages

Michael F. Palopoli, Daniel J. Fergus, Samuel Minot, Dorothy T. Pei, W. Brian Simison, Iria Fernandez-Silva, Megan S. Thoemmes, Robert R. Dunn, and Michelle Trautwein
PNAS first published December 14, 2015; https://doi.org/10.1073/pnas.1512609112
Michael F. Palopoli
aDepartment of Biology, Bowdoin College, Brunswick, ME 04011;
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  • For correspondence: mpalopol@bowdoin.edu
Daniel J. Fergus
bNorth Carolina Museum of Natural Sciences, Raleigh, NC 27601;
cDepartment of Applied Ecology, North Carolina State University, Raleigh, NC 27695;
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Samuel Minot
aDepartment of Biology, Bowdoin College, Brunswick, ME 04011;
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Dorothy T. Pei
aDepartment of Biology, Bowdoin College, Brunswick, ME 04011;
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W. Brian Simison
dCenter for Comparative Genomics, California Academy of Sciences, San Francisco, CA 94118;
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Iria Fernandez-Silva
dCenter for Comparative Genomics, California Academy of Sciences, San Francisco, CA 94118;
eDepartment of Biochemistry, Genetics and Immunology, University of Vigo, 36310 Vigo, Spain;
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Megan S. Thoemmes
cDepartment of Applied Ecology, North Carolina State University, Raleigh, NC 27695;
fKeck Center for Behavioral Biology, North Carolina State University, Raleigh, NC 27695;
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Robert R. Dunn
cDepartment of Applied Ecology, North Carolina State University, Raleigh, NC 27695;
gCenter for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, 2100 Copenhagen Ø, Denmark
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Michelle Trautwein
dCenter for Comparative Genomics, California Academy of Sciences, San Francisco, CA 94118;
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  1. Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved November 12, 2015 (received for review June 26, 2015)

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Significance

Mites live in human hair follicles and have been implicated in medically important skin disorders, but we know surprisingly little about these residents of our skin. By analyzing the variation segregating among 241 mite sequences isolated from 70 human hosts, we showed that hosts with different regional ancestries harbor distinct lineages of mites and that these associations can persist despite generations spent in a new geographic region. These results suggest that some mite populations are better able to survive and reproduce on hosts from certain geographic regions. Improving our understanding of human follicle mites promises to shed light on human evolution and to provide important contextual information for their role in human health.

Abstract

Microscopic mites of the genus Demodex live within the hair follicles of mammals and are ubiquitous symbionts of humans, but little molecular work has been done to understand their genetic diversity or transmission. Here we sampled mite DNA from 70 human hosts of diverse geographic ancestries and analyzed 241 sequences from the mitochondrial genome of the species Demodex folliculorum. Phylogenetic analyses recovered multiple deep lineages including a globally distributed lineage common among hosts of European ancestry and three lineages that primarily include hosts of Asian, African, and Latin American ancestry. To a great extent, the ancestral geography of hosts predicted the lineages of mites found on them; 27% of the total molecular variance segregated according to the regional ancestries of hosts. We found that D. folliculorum populations are stable on an individual over the course of years and that some Asian and African American hosts maintain specific mite lineages over the course of years or generations outside their geographic region of birth or ancestry. D. folliculorum haplotypes were much more likely to be shared within families and between spouses than between unrelated individuals, indicating that transmission requires close contact. Dating analyses indicated that D. folliculorum origins may predate modern humans. Overall, D. folliculorum evolution reflects ancient human population divergences, is consistent with an out-of-Africa dispersal hypothesis, and presents an excellent model system for further understanding the history of human movement.

  • Demodex
  • phylogeography
  • symbiosis
  • coevolution

Footnotes

  • ↵1To whom correspondence should be addressed. Email: mpalopol{at}bowdoin.edu.
  • Author contributions: M.F.P., D.J.F., S.M., R.R.D., and M.T. designed research; M.F.P., D.J.F., S.M., D.T.P., M.S.T., and M.T. performed research; M.F.P., D.J.F., S.M., W.B.S., I.F.-S., and M.T. analyzed data; and M.F.P., R.R.D., and M.T. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession nos. KU174704–KU174944).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1512609112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Global divergence among human follicle mites
Michael F. Palopoli, Daniel J. Fergus, Samuel Minot, Dorothy T. Pei, W. Brian Simison, Iria Fernandez-Silva, Megan S. Thoemmes, Robert R. Dunn, Michelle Trautwein
Proceedings of the National Academy of Sciences Dec 2015, 201512609; DOI: 10.1073/pnas.1512609112

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Global divergence among human follicle mites
Michael F. Palopoli, Daniel J. Fergus, Samuel Minot, Dorothy T. Pei, W. Brian Simison, Iria Fernandez-Silva, Megan S. Thoemmes, Robert R. Dunn, Michelle Trautwein
Proceedings of the National Academy of Sciences Dec 2015, 201512609; DOI: 10.1073/pnas.1512609112
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