S. indica and S. playfairii as sources of
hybridization of S. taiwanensis
The fastsimcoal2 simulation indicated that S. taiwanensis arose
from hybridizations of a ghost lineage with S. indica andS. playfairii approximately 7.62 and 4.77 kya,respectively, suggesting multiple origins of extant S.
taiwanensis . Older specimens of S. taiwanensis are often
mistaken morphologically for S. indica , and the habitat ofS. taiwanensis on shady slopes is similar to that of S.
playfairii (Hsieh & Huang, 1995). Despite this multiple-source
hybridization, S. taiwanensis is considered a single species
since the two hybrid lineages (TAI1 and TAI2) are monophyletic in
multispecies coalescent (ASTRAL) inferences. Hybridization events may
displace certain gene trees, leading to gene tree incongruence or
topological inconsistencies between multispecies coalescent and
concatenated analyses (Degnan & Rosenberg, 2009), as supported by the
low F ST with other indica group members
(Fig. S3A). Approximately 60% of the genetic components of S.
taiwanensis are from indica group members.
S. taiwanensis is scattered in the shallow mountains of southern
Taiwan and partially overlaps with S. playfairii , enabling
hybridization between the ancestor of S. taiwanensis (ghost
lineage) and S. playfairii . Surprisingly, S. taiwanensishybridized with S. indica , a species that has no distributional
overlap with S. taiwanensis and is distributed in north-central
Taiwan. In addition to long-distance dispersal, we cannot exclude the
possibility that an ancestor or close relative of S. indicaspread to the south (Chiang, Huang, & Liao, 2012) and hybridized withS. taiwanensis after the glacial climate began. Although the
middle and low altitudes of Taiwan Island did not experience glacial
coverage, the arid and cold glacial climate forced many organisms to
hide in multiple relict refugia during the Pleistocene glacials. In
Taiwan, glacial refugia are commonly found in mountainous areas in the
south or southeast (Huang, Hwang, & Lin, 2002; Lee et al., 2006; Wu et
al., 2006) and Mount Sylvia (Xue-shan) in the northeast (Cheng, Hwang,
& Lin, 2005; Huang, Hwang, & Lin, 2002; Lee et al., 2006; Wu et al.,
2006). The warm and humid southern mountains of Taiwan served as a
glacial refugium for numerous species, including Castanopsis
carlesii (Cheng, Hwang, & Lin, 2005), Quercus glauca (Huang,
Hwang, & Lin, 2002; Lee et al., 2006), Cinnamomum kanehirae(Liao et al., 2010), and Machilus kusanoi (Wu et al., 2006),
resulting in high genetic diversity.
During the refuge period, hybridization between closely related species
may have occurred. A previous study showed that the Pleistocene glacial
oscillations accelerated Scutellaria species interbreeding in
southern Taiwan and that current environmental heterogeneity is
responsible for shaping the genetic structure of Scutellariapopulations (Huang et al., 2017). Due to this genetic legacy, glacial
refugia in southern Taiwan contributed to genetic diversity in extant
populations. Genetic mixing in refugia in the south may have been
delayed until the postglacial period (ca. 7-4 kya from ABC). This
inference is supported by the fact that demography explains more than
half of the adaptive genetic variation, whereas the current climate
explains only a small share. This result suggests that demographic
history, such as changes in population size and gene flow, was crucial
in shaping the genetic structure of the current population/species.
The spread of beneficial genes may broaden the ecological niche or
enable hybridized species to colonize novel habitats (Suarez-Gonzalez et
al., 2018). We identified two adaptive genes involved in the
introgression between S. taiwanensis and each of the potential
hybridized species: PHYB (between S. taiwanensis andS. indica ) and OPCL1 (between S. taiwanensis andS. playfairii ). PHYB was associated with the mean diurnal
range (BIO2), and S. indica was present within a broad range of
BIO2, suggesting that this species can acclimate to a diverse
distribution of habitats and tolerate large temperature variations
within a year. PHYB has been shown to promote plant adaptation to
cold environments (Jiang et al., 2020; Zhao et al., 2016). The
introgression of PHYB between S. indica and S.
taiwanensis may have enabled S. taiwanensis to colonize and
thrive in southern Taiwan. OPCL1 was associated with several
temperature and precipitation-related factors, including the mean
diurnal range (BIO2), temperature seasonality (BIO4), maximum
temperature of the warmest month (BIO5), minimum temperature of the
coldest month (BIO6), temperature annual range (BIO17), and
precipitation of the warmest quarter (BIO18). Among these environmental
variables, variations in BIO5 were larger in the habitats of S.
playfairii than in the habitats of S. taiwanensis . The
transmission of alleles of OPCL1 may further increase the
adaptability of S. taiwanensis to lower temperatures in warm
seasons compared to most Scutellaria species in Taiwan except forS. hsiehii . However, the niches of S. taiwanensis differed
from those of either potential hybridized species and were characterized
by lower BIO4, higher BIO6, and higher BIO18, indicating a shift toward
temperature- and precipitation-related traits associated with tropical
climates in southern Taiwan. Alternatively, these differences could
indicate relics of ancestral traits of ghost lineages that are not
related to the hybridization events. Overall, we infer that climate
drivers of the introgression of adaptive alleles combined with
demographic history associated with climate oscillation generated the
unique genetic components and high genetic diversity of S.
taiwanensis .