Introduction
The study of organisms that are obligately or facultatively associated
with humans can provide insight into the history of its host. For
example, human head lice have been used as markers of the past to
uncover prehistoric contact between extinct and anatomically modern
humans (AMH) (Reed et
al., 2004), the timing of the split between human and chimpanzees (5-7
Ma) (Reed et al., 2007), and the origin of clothing use by AMH (Kittler
et al., 2003; Toups et al., 2011). The human head louse Pediculus
humanus capitis De Geer, 1778 (Phthiraptera: Anoplura) is a permanent,
blood-feeding ectoparasite of humans completing their entire life cycle
on their human host. Lice cannot live off their host for more than 36
hours (Burkhart & Burkhart, 2007), making their life cycle closely tied
to their hosts for thousands of generations. Head lice are primarily
found among school-aged children and dispersal (transmission) from one
head to another occurs mainly when the host individuals have close
physical contact (Mumcuoglu et al., 2021). Ancient human populations
also carried lice, and this is demonstrated by the finding of nits still
attached to ancient human hair as well as trapped in the combs used
(Amanzougaghene et
al., 2016; Arriaza et al., 2014; Pedersen et al., 2022). Therefore,
host migration and contact should define the population structure of
lice. Historically, this appears to be true, that the evolutionary
history of human lice appears to have been shaped by human migration
(Ewing, 1926; Pedersen et al., 2022) that facilitated host-switching
(Reed et al., 2007). However, the increase in ease of global migration
and travel could break down geographical barriers and erase historical
population structure. The question remains, is louse population
structure defined by geographic regions and historic migration or recent
host movement.
Anatomically modern humans migrated out of Africa 60-70 thousand years
ago (Carto et al., 2009; Stringer, 2000; Walter et al., 2000). A growing
number of studies now support two main dispersal events out of Africa: a
Southern route to Southeast Asia and a Northern route to Eurasia
(Reyes-Centeno et al., 2014; Tassi et al., 2015). As AMHs dispersed
throughout Eurasia they interbred with other species of archaic humans
including Neanderthals and Denisovans who migrated out of Africa much
earlier (Reich et al., 2011; Sankararaman et al., 2014; Villanea &
Schraiber, 2019). While genetic and archeological evidence has increased
our understanding of human evolution, a complete picture remains elusive
because behavior and dispersal are hard to discern from fossilized
remains.
As speciation happens in the host lineage, host-specific parasites like
lice often speciate in tandem as a result of imposed isolation (Reed et
al., 2007). Therefore, the processes shaping human evolution may leave a
signal in the genome of human lice. To date, genetic diversity and
population structure of head lice has mostly been examined in terms of
mitochondrial clade diversity and distribution (Al-Shahrani et al.,
2017; Amanzougaghene et al., 2016; Ashfaq et al., 2015; Boumbanda Koyo
et al., 2019). Mitochondrial genes; partial cytochrome b and cytochrome
oxidase I of lice showed six genetically distinct, geographically unique
clades (clades A-F). Clade A is distributed world-wide, while the other
clades are more geographically restricted. Clade B is found in Europe,
the Americas, and Australia. Clade C is found in Africa and southern
Asia. Clades D and E are found only in Africa, while Clade F has been
found on individuals in Argentina and Mexico (Amanzougaghene et al.,
2019). Of these clades, only A and D include both head and body lice,
while the rest of the clades have consisted only of head lice.
Although identifying the distribution of mitochondrial clades through
only fragments of genes has helped elucidate the possibility of a
demographic history of human head lice, these patterns are only vaguely
indicative of just the maternal louse lineages, and longer term
co-speciating and coevolutionary events. An understanding of genome-wide
patterns of genetic diversity and population structure across global
head louse populations are needed to characterize the complete picture
of louse evolutionary history. For example, considering that lice are
horizontally transmitted, it is unclear if the nuclear genetic structure
of the lice mirrors that of its host genetic population structure, or if
human migrations and more recently the ease of global travel has erased
these patterns by transporting lice around the world. The question
remains whether lice are more defined by geography or host movement.
Given the long history of human migration across the globe, and the
co-demography observed in lice (Reed et al., 2007), it is useful to
evaluate worldwide louse populations as geographical units (i.e.,
countries or continents) rather than genetic clades. Investigating
population structure across geographically separated populations using
neutral nuclear loci can show interactions between genetic drift and
gene flow (Slatkin, 1987) that may not be captured by uniparentally
inherited markers (i.e., mitochondrial DNA) (Ebert & Fields, 2020).
In attempts to understand the nuclear genetic diversity of human lice, a
previous study used microsatellite markers from 93 specimens in 11
countries and found no relationship between the mitochondrial clades and
the nuclear population clusters (Ascunce et al., 2013). Additionally,
these microsatellite markers were able to detect geographically
structured genetic population clusters indicating low levels of gene
flow between global louse populations (Ascunce et al., 2013). Further
investigations with a much broader sampling regime including genome-wide
representation are needed to have the resolution to identify the
distribution of genetic variants as well as the genetic population
structure of the global human head louse populations.
Using the human body louse, Pediculus humanus humanus genome as a
reference, we analyzed whole nuclear genomes of the human head louseP. humanus capitis from across the world to overcome the current
lack of geographic and genome-wide representation. The main goals of
this study were to: 1) investigate nuclear genetic diversity across the
globe ; 2) examine the geographic distribution of genetic variants
worldwide ; 3) identify the population structure based on nuclear
markers; and 4) investigate possible modes of gene flow and historical
population connectivity between global louse populations. Our main
questions are, does the population structure of human lice match that of
its host migration patterns or does it reflect the same evolutionary
history shown through its mitochondrial genome?