Introduction
Population genetics within a host-parasite association are complex
systems dependent on many ecological features of both counterparts
(Criscione, Poulin, & Blouin, 2005; Barrett, Thrall, Burdon, & Linde,
2008; Sweet & Johnson, 2018). Within hybrid zones (HZ) and secondary
contact zones (SCZ) this picture is likely to become even more
complicated, possibly giving rise to new unexpected patterns.
Unfortunately, very few studies have been devoted to this aspect of
host-parasite interactions. From the most general point of view, it is
assumed that since parasites are dependent on their host, their genetic
structure will tend to mirror the host. In this respect, two assumptions
are frequently expressed. First, the degree of congruence with the host
is dependent on traits connected to the parasitic life-style, such as
the degree of host-specificity, transmission mode, presence of dispersal
stages, etc. (Maze-Guilmo, Blanchet, McCoy, & Loot, 2016). Generally,
the more intimate the association, the higher the degree of congruence.
However, this general view may be twisted by many specific traits of the
particular host-parasite association. For example, the population
structure of heteroxenous parasites (parasites with more than one host
in their life cycles) is likely to reflect the least structured host,
since any potential structure is erased by the more motile host (Jarne
& Theron, 2001;
Louhi,
Karvonen, Rellstab, &
Jokela,
2010). Similarly, with longer free living stage(s), the genetic
structures of the host and the parasite become more incongruent (Jarne
& Theron, 2001). The second assumption is about the speed of
diversification: since the parasites have a shorter generation time,
they undergo faster genetic diversification, which may eventually lead
to the parasite’s duplication
(Page,
Lee,
Becher, Griffiths, & Clayton, 1998; scenario a in Figure 1).
The assumption about the higher mutation rate in parasites was
demonstrated in several studies (Nieberding, Morand, Libois, & Michaux,
2004; for ectoparasites: McCoy et al., 2005; Whiteman, Kimball, &
Parker, 2007; but see Gómez-Díaz, González-Solís, Peinado, & Page,
2007; Jones & Britten, 2010 for the opposite results).
Although many studies have been devoted to comparing phylogenies and
population structures of host-parasite associations, only a few analyzed
these processes in connection to SCZ and HZ of the hosts (reviewed by
Theodosopoulos, Hund, & Taylor, 2019), and only recently, de Bellocq et
al. (2018) focused on detecting HZ in parasite populations. Using two
parasites of the house mouse Mus musculus , the nematodeSyphacia obvelata and the fungus Pneumocystis murina , they
found that within the host’s HZ both parasites create their own HZ. They
also demonstrated that the parasites (reaching higher genetic
divergence) created significantly narrower HZs than the host (scenariob in the Figure 1).
From a theoretical point of view, the assumptions and empirical evidence
discussed lead to a third possible scenario: during secondary contact
the host does not create a HZ but rather re-establishes a panmictic
population, while the parasite accumulates a degree of genetic
differences which prevent re-establishment of panmixia but does not lead
to speciation (scenario c in the Figure 1). A paradoxical result
of such an event would be establishment of a parasite’s HZ within the
host’s panmictic population, which on a microevolutionary scale would
function as a “host-cleansing filter”: passing through this filter
from area A to area B (Figure 1d), the hosts rid themselves of area A
parasites and acquire the area B parasites. To our knowledge, this
“filter” has never been observed in nature. In fact, the presence of a
parasite’s HZ in the scenario described here is difficult to guessa priori , as it is not indicated by the host’s HZ. However, in
our previous work (Martinů, Hypša, & Štefka, 2018) we presented the
genetic structure of postglacial Europe recolonization by the mice of
the genus Apodemus and their ectoparasite, the lousePolyplax serrata , which corresponds to such scenario (Figure 2;
see below for details).
Similar to all sucking lice, P. serrata is a permanent homoxenous
ectoparasite with strict host specificity, which is transmitted almost
exclusively during physical contact of its hosts. As such it falls into
the category of highly intimate parasites displaying a high degree of
congruence with their hosts. In Figure 2, we summarize the main features
of the population genetic pattern obtained by analysis of 379 bp
mitochondrial haplotypes (Martinů et al., 2018). It shows that P.
serrata is composed of several genetic lineages (Figure 2d) with
different host-specificities and geographic distributions. This
indicates that even such traits as the degree of host specificity may be
very flexible and change rapidly at a shallow phylogenetic level. For
example, the so-called specific (S) and non-specific (N)
lineages, although closely related (sister lineages) and living in
sympatry, differ in degree of their specificities, one being exclusive
to Apodemus flavicollis, while the other can also live onA. sylvaticus . However, the most intriguing part of the pattern
was detected within the S lineage. On the mtDNA based phylogenetic
trees, the host (A. flavicollis ) and the parasite (S-lineage ofP. serrata ), display the same basic structure. Their samples
collected across all of Europe form two genetically distant clusters,
suggesting recolonization from two different refugia (the taxa
designated by red and blue colours in the Figure 2; see Martinů et al.,
2018 for discussion). However, while the two host’s clusters have
already spread across the entirety of Europe, their lice did not follow
the same process. Instead, their two sub-lineages, designated asspecific east (SE) and specific west (SW), ceased their
dispersion after reaching the SCZ in the middle of Europe (Figure 2).
This disparity is surprising since the high intimacy of lice should
predetermine them to mirror genetic structure of the host (e.g. Harper,
Spradling, Demastes, & Calhoun, 2015).
To obtain a more complex picture of secondary contact in P.
serrata , in this study we analyze three patterns derived from
metagenomic data of 13 louse specimens collected across the SCZ: nuclear
SNPs, complete mitochondrial genomes, and complete genomes of the
symbiotic bacterium Legionella polyplacis . We use these analyses
to retrieve two kinds of information. First, we compare nuclear and
maternally inherited markers (mitochondrial genomes, symbiotic genomes)
to demonstrate a narrow HZ between the SW and SE lineages of the lice.
Second, we address two possible causes of the SE/SW incompatibility
suggested in our previous work (Martinů et al., 2018). P. serratacarries the intracellular obligate symbiont Legionella polyplacis(Říhová, Nováková, Husník, & Hypša, 2017) which could be incompatible
with the non-native genetic background. Similarly, since thePolyplax louse mitochondria are fragmented into 11
minichromosomes (Dong, Song, Jin, Guo, & Shao, 2014) a rearrangement of
their genetic composition could theoretically lead to the SE/SW
incompatibility. We therefore compare complete mitochondrial and
symbiotic genomes to assess the degree of their divergence.