Genetic variation in filtering force of mutualistic partnerships
Despite symbiosis filtering to favor specific genotypes, genetic
diversity of Frankia was high in the rhizosphere soil under a
host plant. Consistently, previous studies have found that genetic
variation in mutualistic partners is sustained in nature (Barrett et al,
2015; 2016; Clawson et al., 1998; 1999; Huguet et al., 2001; Põlme et
al., 2014). However, stabilizing mechanisms alone cannot explain the
persistence of the variation because the evolutionary fixation of the
most beneficial partner genotypes is predictable (Heath & Stinchcombe,
2014; Law & Koptur, 1986; Parker, 1999; Weyl et al., 2010).
Furthermore, the fixation of the beneficial genotypes may lead to the
loss of discrimination ability by hosts if it needs a cost (Foster &
Kokko, 2006; Frederickson, 2013; Heath & Tiffin, 2009; McNamara &
Leimar, 2010). One solution to this paradox is mutation-selection
balance (Heath & Stinchcombe, 2014): the hypothesis that variation in
partner quality is maintained by the balance in mutation, which
introduces genotypes of lower quality, and selection, which acts to
favor the partner genotypes of higher quality. Genetically diverse pool
and strong filtering for symbiosis found in this study supports the
mutation-selection balance hypothesis. This study suggests
mutation-selection balance in the field. Future studies should pay
attention to quantifying the strength of selection that stabilizing
mechanisms impose on partner quality in nature. This would provide great
insights for an understanding of the evolution of partner quality and
the maintenance of genetic diversity in symbiosis (Heath & Stinchcombe,
2014).
This study quantified the symbiosis filtering force using a community
dissimilarity approach and found the possibility of genetic variation of
hosts in the filtering forces in the field (Fig. 3). The reason why
similar bacterial compositions were sustained among almost all alders in
spite of the variation in the filtering force among host individuals is
likely to be explained by the spatial heterogeneity in genetic diversity
of Frankia . Frankia genotypes are heterogeneously
dispersed in forests (Kagiya and Utsumi 2020). Additionally, NMDS
revealed the high variation of Frankia composition in rhizosphere
soils among host individuals (Fig. 2a). The necessity of filtering force
could depend on genetic diversity and/or the relative abundance ofFrankia genotypes in the surrounding local soil. In fact, the
genetic community structure of bacterial symbionts in the host’s
rhizosphere soil differed in line with soil nutrients, whereas no
effects of genetic variation in a host plant were detected to shape
rhizospheric bacterial communities (Table 1). If the ability of
filtering requires costs and a common optimal symbiont composition is
consistent among host individuals, the balance between the necessity and
costs can maintain the homogeneity of symbiont composition in a host
plant along with genetic variation in filtering force.
The variation in filtering force might also contribute to the
maintenance of genetic variation in microsymbionts. When variation in
stabilizing mechanisms alters selection pressure for microsymbionts,
genetic variation in microsymbionts, even those involving lower quality
genotypes, may be sustained (Heath & Stinchcombe, 2014). For example,
some studies have reported that sanctions are not perfectly effective
because they cannot respond to non-zero benefit levels or cannot punish
individual partner genotypes (Charlotte et al., 2012; Kiers et al.,
2006). If genetic variation in a host plant alters the strength of
symbiosis filtering, genetic variation in the host will be the key to
revealing coevolution in mutualistic interactions under natural
ecosystems with a high genetic diversity of microsymbionts.
The present study clearly demonstrates that host plants interact with
specific symbiont genotypes via symbiosis filtering in the field. Our
finding that symbiosis filtering indices correlated with the genetic
distance of hosts is likely to be evidence of linkage between host
genetics and symbiont assembly in nature, even if symbiosis filtering
indices depend on the dissimilarity of Frankia composition in
rhizosphere soils among rivers and/or non-infective strains that make upFrankia communities in rhizosphere soils. Toward an integrative
understanding of mutualistic coevolution and community assembly in
natural ecosystems, future studies should pay attention to differences
in partner quality and infectivity between infecting and non-infecting
members of communities. Moreover, revealing the genetic basis underlying
stabilizing mechanisms is fruitful toward an understanding of the
interplay between coevolutionary dynamics in mutualism and community
assembly in symbiosis.