Evidence of parallel evolution in several warm-temperature
adaptation genes
In general, geographically distinct populations that are exposed to
similar environmental conditions evolve similar genotypic and phenotypic
traits. The replicated nature of S. japonica provides clear
molecular signatures that can be used to recover many alleles
consistently associated with parallel warm-temperature adaptations
between the ZS and IB/TB populations. In the present study, most genes
(91.0%) associated with local warm-temperature adaptation in the Japan
populations were shared with selection genes in the ZS population, in
which the populations spanned long geographic distances and showed a
similar annual temperature (19.1 ℃–21.3 ℃). However, the selection
genes in the Japan populations did not overlap with the high-temperature
adaptation genes in the ST population. The integration of the shared
selection genes and similar temperature environments could be considered
as a possible evidence for parallel evolution in S. japonica . The
PCA results based on the SNPs of the shared selection genes revealed
close but distinguishable patterns between the ZS and two Japan
populations, indicating independent selection events on the same genes
between the ZS and IB/TB populations. A similar conclusion was reported
for the three spine stickleback. Fixation of different loci at the same
gene was observed in marine–freshwater divergence of threespine
stickleback (Barrett, Rogers, & Schluter, 2008). Evidence of parallel
evolution at the TSHR gene was observed between the Atlantic
herring populations from both sides of the Atlantic Ocean. TSHRis a major gene associated with the timing of reproduction (Lamichhaney
et al., 2017). Parallel genetic evolution was also reported in the
Atlantic cod and Sebastiscus marmoratus (Xu et al., 2017;
Bradbury et al., 2010).
In the present study, S. japonica provided an opportunity to
study the genetic basis of repeated parallel evolution in geographically
distant populations. The results offered a chance to identify the
warm-temperature adaptation genes in different independent populations.
Candidate genes were identified within peaks of parallel divergence
between the ZS and IB/TB populations. These candidate genes may be
important for adaptation to warm temperature. The GO clusters were
primarily enriched in the categories of cell projection, structure of
the cytoskeleton, protein binding, maintenance of membrane, and cell
differentiation. However, no significantly enriched KEGG pathways were
detected. The top 20 enriched pathways were related to metabolism
(synthesis and degradation of ketone bodies, cyanoamino acid metabolism,
linoleic acid metabolism, alpha-linolenic acid metabolism, and butanoate
metabolism), circulatory system (vascular smooth muscle contraction),
and endocrine system (salivary secretion and pancreatic secretion).
Given that S. japonica is a species adapted to warm temperatures,
the warm temperature had a relaxed selective pressure on the genes
involved in response to heat stress. Moreover, the warm temperature
promoted the growth of S. japonica by increasing the fluidity of
the cell membrane and requiring rapid cell division and frequent
extracellular and intracellular exchange of substances. Among the
candidate genes for warm-temperature adaptation, four genes were located
in the GO term cell division (GO: 0051301), 17 genes were involved in
the cytoskeleton (GO: 0016328), 10 genes were located in GO term
transmembrane signaling receptor activity (GO: 0004888), and 8 genes
were located in GO term ion transmembrane transport (GO: 0034220).
Various receptors in the membrane and ion transmembrane transport genes
have important roles in the material exchange between the inside and
outside environments of cells to satisfy the requirement for rapid cell
division. Furthermore, three genes (FMN2 , MGMT , andPOLH ) were located in the GO term DNA repair (GO: 0006281),
thereby avoiding DNA replication errors. FMN2 plays a role in
responding to DNA damage, cellular stress, and hypoxia by protecting
CDKN1A against degradation. FMN2 also promotes the assembly of
nuclear actin filaments in response to DNA damage to facilitate the
movement of chromatin and repair factors after DNA damage (Yamada, Ono,
Perkins, Rocha, & Lamond, 2013). MGMT is crucial for genome
stability. It repairs the naturally occurring mutagenic DNA lesion
O6-methylguanine back to guanine and prevents mismatch and errors during
DNA replication and transcription (Kawate et al., 2000). POLHserves as a DNA polymerase specifically involved in DNA repair by
translesion synthesis (Masutani et al., 1999). Warm temperature promotes
material exchange, DNA replication, and cell division. Suitable
temperature ensures that enough food resources are available in the
environment. Hence, these terms are functionally necessary for the
adaptations of S. japonica to warm temperatures.