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

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.

Keywords: Demodex; coevolution; phylogeography; symbiosis.

Fig. 1.

Maximum likelihood (ML) tree of D. folliculorum mtDNA (883 bp, 70 hosts, 241 sequences). Dots indicate the continent on which a host was born (note that Latin American regions Mexico and Central America are grouped with South America). Colored rectangles above each dot indicate the host’s continental ancestry. Rectangles of mixed colors indicate mixed parental ancestry. Red stars indicate bootstrap (BS) values and posterior probabilities (PP) are >0.90 from both ML and Bayesian analyses. Gray stars indicate nodes where only Bayesian posterior probabilities are >0.90. Multiple sequences from a single host that were either identical or clustered together in a single clade were collapsed into a single tree tip. See Figs. S1–S3 for alternative representations of this phylogeny. We recovered four major clades that differ in relative frequency depending on the geographic origins of the hosts. The great majority of hosts with European ancestry are included in clade D; clades A, B, and C primarily include hosts of African, Asian, and Latin American ancestry. A light micrograph of a D. folliculorum female is shown in the center.

Fig. S1.

Bayesian version of Fig. 1 with all the original sequences represented (i.e., multiple sequences from a single host that were either identical or clustered together in a single clade were retained in this representation of the phylogeny). A light micrograph of a D. folliculorum female is shown in the center. At the bottom is an unrooted version of this phylogeny for comparison. BS, maximum likelihood bootstrap value; PP, Bayesian posterior probability.

Fig. S2.

Alternative representations of the phylogenetic information depicted in Fig. 1. (Upper) An unrooted version of the ML tree. (Lower) A Neighbornet network that visually represents the conflicting phylogenetic signal in our dataset.

Fig. S3.

Bayesian phylogeny based on mitochondrial COIII sequences with individual hosts highlighted. Host 206 (blue text) was sampled 36 times over the course of 3 y (2007–2009), and the same D. folliculorum COIII haplotypes were recovered from host 206 each year. The year is indicated by the suffix 7, 8, or 9. Three family groups (here labeled 1, 2, and 3), each including a mother, father, and offspring of European ancestry, were sampled also. Spouses, parents, and offspring share D. folliculorum COIII haplotypes much more often than do unrelated hosts.

Fig. 2.

Frequency of clade recovery according to the geographic region of host ancestry. Clades A, B, C, and D were recovered from African and Latin American hosts; Asian participants hosted only clades A, B, and D; Europeans primarily hosted mites from clade D. Sequences with missing data were excluded from host and haplotype counts.