| 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.Human evolution did not take place in isolation but instead occurred alongside that of many closely associated species. Phylogeographic studies of human-associated species—such as lice and rodents, as well as certain bacteria and viruses—have suggested, eliminated, and confirmed hypotheses about human history (1–10). For example, these studies have provided details about the timing and nature of the original human migration out of Africa, the spread of humans within and among continents, and the domestication of large vertebrates.Mites of the genus Demodex live in the hair follicles and sebaceous glands of humans and provide a promising system with which to explore further the details of human evolution. The association between Demodex and Homo sapiens is likely to be an ancient one: The broad distribution of these mites across mammal species (11), coupled with the ancient date of divergence estimated between the two species known to be found on humans (12), suggests that Demodex originated and diversified with early mammals. Furthermore, Demodex seem likely to have been carried along whenever their hosts migrated, because they are ubiquitous inhabitants of human skin (13, 14). Finally, in comparison with the other human associates that have been studied to date, Demodex mites are more tightly associated with human bodies than are lice, while their generation times are slower than those of bacteria and viruses but are faster than those of rodents, making them a complementary system with which to understand the evolution of both humans and human associates.Two species of Demodex are known to inhabit the skin of humans. Histological studies suggest that each occupies a different niche: Demodex folliculorum resides in the hair follicle and is often found near the skin surface, whereas Demodex brevis is generally found deep in the sebaceous glands (15). As a result, the frequency of D. folliculorum movement from one host to another may be greater than that of D. brevis. A recent phylogenetic analysis of Demodex, including the two human associates, shows geographically structured genetic variation in D. brevis in which individuals of European descent and those of temperate Asian (Chinese) descent exhibit up to 6% divergence in nuclear ribosomal 18S sequence (14). In contrast, studies based on 18S rDNA and 16S mtDNA suggest that D. folliculorum exhibits no clear geographic structure among hosts from China, Spain, Brazil, and the United States (14, 16, 17). However, without additional sampling it is impossible to know whether the absence of apparent geographic structure in D. folliculorum truly reflects high rates of global gene flow or instead is an artifact of limited global sampling and the particular genetic loci studied.Key to understanding the global phylogeography of these mites is an understanding of how they move among hosts. The transfer of mites from mother to progeny and between mating partners has been demonstrated in nonhuman mammals (18–21). However, the movement of Demodex among human hosts has not been characterized. If human mites are transferred between hosts at high rates, the resulting high rates of migration could account for the limited geographic structure observed in D. folliculorum to date.Here we used a 930-bp fragment of the mitochondrial genome to evaluate the genetic diversity and phylogeography of D. folliculorum among 70 human hosts of diverse geographic origins and ancestries. Our samples included people of European, Asian, African, and Latin American descent, the majority of whom currently live in the United States, providing the most broadly sampled evolutionary tree to date for any Demodex species.Additionally, we investigated Demodex transmission among humans in two ways. First, we sampled multiple mites from a single host individual over the course of 3 y to characterize the diversity and stability of the mite population. Second, we examined the relationships among mites on three sets of parents and their adult progeny; because of the close association among family members, we hypothesized that mite lineages are more likely to be shared within families than between unrelated hosts.The study of Demodex mites speaks to the story of human evolution as well as the coevolution between symbiont and host. Moreover, understanding these mites and their microbes will have applied value, because they have been linked to skin disorders such as rosacea and blepharitis (22, 23). Whatever the influence of mites on these disorders may be, it may depend on the mite lineages inhabiting a particular host. Ultimately, elucidating the evolution and transmission of Demodex mites not only will be a useful step toward understanding the evolutionary history of humans but also will be critical to contextualizing their role in human health. |
