Discussion
Hybridization results in variation with new combinations of alleles
through the same mode of sexual reproduction in species,
which
may provide a basis for adaptive evolution
(Abbott et al. 2013). However,
sexual reproduction can result only in nuclear gene recombination,
whereas cytoplasmic genes are maternally inherited
(Birky 2001;
Greiner et al. 2015). Thus,
asymmetric gene flow between cytoplasmic and nuclear loci is considered
to provide evidence of interspecific hybridization
(Setoguchi& Watanabe 2000). Our results
showed that R. flaviceps and R. chinensis exhibited
asymmetric genetic differentiation between their mitochondrial and
nuclear genes. There was low gene flow and high genetic divergence of
mitochondrial genes, while there was high gene flow and low genetic
divergence of nuclear genes between the species.
Additionally, the identifiedR. flaviceps/R. chinensis colonies possessed R.
chinensis/R. flaviceps nuclear genes. These results suggested that
interspecies hybridization and gene exchange occurred in the two termite
species in nature.
What are the possible factors causing hybridization? In termites, the
overlap of the
distribution
and swarming of related species is common, and the sex-pairing pheromone
is similar in sibling species (Aldrich&
Kambhampati 2009; Capblancq et al.2015; Hartke& Rosengaus 2011). More
importantly, neither males nor females possess external sclerotized
genitalia (Hartke& Baer 2011). Thus, the
indicated prezygotic reproductive barrier may be largely absent in some
sibling termite species. Second, the initial colony is usually
established under monogamy (Korb&
Hartfelder 2008; Thorne et al.1999). Many monogamous individuals may fail to mate with conspecific
partners due to the sex ratio, predators and/or other factors
(Matsuura et al. 2002). In this
case, their mating with heterospecific partners and nest building favour
improved fitness when they encounter each other. Additionally, in some
subterranean termites, workers can develop into secondary reproductives
(Haverty& Howard 1981;
Su et al. 2014), and dealates that
fail to mate can also live for a long time; they may find a homosexual
partner and co-establish a stable nest
(Mizumoto et al. 2016). Hence, it
is possible that foraging workers fuse to form a heterospecific virgin
colony and then mate with heterosexual dealates, which provides a
possible mechanism for hybridization between dealates and secondary
reproductives developing from workers.
Adaptive introgression of genetic material between incompletely isolated
species may cause various impacts on genetic diversity. It can
contribute to genetic diversity or facilitate genetic assimilation
depending on the size and construction of populations
(Seehausen 2004). For social termites,
many colonies are established by founders from the same natal colony
(DeHeer& Vargo 2005;
Vargo& Husseneder 2009). One closed
colony can be composed of kin, which may lead to inevitable inbreeding.
In fact, high genetic diversity is still maintained in natural
populations (Huang et al. 2013;
Vargo& Husseneder 2009). Fortunately,
hybridization and introgression between incompletely isolated species
may explain why genetic diversity can be maintained in natural
populations of termites with respect to inbreeding. We previously noted
that R. flaviceps and R. chinensis possess similar
behaviours and lack conspecific preferences in the process of
reproduction (Wu et al . 2019). At
the same time, we found that artificial hybrid colonies can produce
living offspring under laboratory conditions. Combined with the results
regarding genetic exchange between the species in nature in this study,
we further confirmed the speculation that the maintenance of high
genetic diversity in termites is related to adaptive introgression and
hybridization.
In general, incomplete reproductive barriers occur in young species
because they remain in the initial stage of differentiation. For
example, a host shift led to prezygotic reproductive isolation between
the original species and host races in Rhagoletis pomonella , but
the postzygotic reproductive barriers were invalid due to the short time
of differentiation (Dambroski& Feder
2007). However, hybridization between long-diverged species often
negatively affects the
viability
and fertility of hybrid offspring, preventing gene flow between species
(Anderson et al. 2010;
Brideau et al. 2006;
Brucker& Bordenstein 2013;
Fitzpatrick 2008;
Moyle& Nakazato 2009). Inconsistent with
that prediction, the differentiation time between R. flavicepsand R. chinensis is 2-3 million years
(Bourguignon et al. 2016). Our
results indicated that they exhibit incomplete reproductive barriers and
that there is gene flow between the two species. Similar patterns of
gene exchange are also reported in the related tapeworm speciesSchistocephalus solidus and S. pungitii despite their
differentiation 20-25 million years ago
(Henrich& Kalbe 2016). These results
suggested that interspecific gene exchange shows not relationship with
the time of species differentiation.
During the process of evolution and speciation, differentiated species
are often re-fused due to diffusion or environmental changes, which can
result in adaptive introgression or speciation via hybridization. The
phylogenetic relationship of this evolutionary process cannot be
described through
a
binary bifurcation structure but by a network, namely, reticulate
evolution. Therefore, the existing phylogenetic tree based on a binary
bifurcation structure cannot truly describe the evolution of species
(Pennisi 2016). Additionally,
hybridization can reduce differences between taxa or even cause a
genetic homogenizing effect (Bernalet al. 2017; Schierenbeck 2011).
Alternatively, hybridization results in the introgression of genetic
material and accelerates speciation (Abbottet al. 2013; Bendesky et al.2017; Payseur& Rieseberg 2016).
However, hybridization and gene introgression existed in the termiteReticulitermes (Dedeine et
al. 2016). Neither the above-described reductions in genetic
differences between species nor speciation are observed in the termiteReticulitermes . If this were the case, there would clearly be
strong selection against hybridization to maintain species integrity in
nature. Further studies on the maintenance mechanisms of species will
still be required in the future.