Introduction
Introgression
is vital for plant evolution (Arnold, 1997; Rieseberg & Wendel, 1993;
Villa‐Machío et al., 2023). The outcome of introgression depends on the
taxa, environmental conditions, and degree of differentiation (Abbott et
al., 2013). Introgression can break species boundaries and result in
genetic homogenization, but it can also introduce genetic variations
that may lead to divergence and promote speciation along with
adaptation.
Introgression between closely related species is most likely to occur
under secondary contact, which has
diverse consequences for speciation. Genetic recombination caused by
hybridization can reshape the new species and isolate it from its
parents; for example, in grasshoppers, a hybrid swarm facilitated the
persistence of reproductive isolation from the parental species
(Noguerales & Ortego, 2022). Interbreeding can also provide a reservoir
of standing genetic variation that produces a wide range of adaptive
outcomes (Barrett & Schluter, 2008), such as adaptive introgression
across species boundaries, in which beneficial genetic elements are
transferred between species through hybridization (Suarez-Gonzalez et
al., 2018). Detecting the levels, directions, and drivers of
introgression is essential for understanding the speciation mechanisms
of related species on islands. However,
incomplete lineage sorting (ILS), in
which alleles from a common ancestor, i.e., ancestral polymorphisms, are
randomly retained, could leave a signature of genetic admixture similar
to that of introgression (Buckley et al., 2006; Du, Petit, & Liu, 2009;
Funk & Omland, 2003). Therefore, these two nonexclusive mechanisms must
be distinguished and quantified to unravel the speciation pattern of a
species complex (Funk & Omland, 2003; Hedrick, 2013).
In some environments, such as island habitats, local adaptation is
crucial for maintaining species integrity (Algar & Mahler, 2016; Huang
et al., 2016a). Islands have intrigued taxonomists, evolutionists, and
ecologists since Darwin because, as closed or semi-closed restricted
areas, they offer more opportunities for introgression, facilitatingin situ diversification (Ellepola et al., 2022; Ye, Yang, &
Tian, 2023). When isolated
populations encounter diverse and unique island environments, they face
distinct selection pressures that lead to adaptive divergence. This
process involves the accumulation of genetic variations that enhance the
ability of these species to survive and thrive in their specific
habitats (Exposito-Alonso, 2023; Lasky, Josephs, & Morris, 2023). For
rapidly diverging species with small population sizes, local adaptation
takes on increased importance because it acts in conjunction with
non-adaptive drivers, such as random genetic drift (Wiens et al., 2022),
to strengthen the genetic differentiation between populations (Rosche et
al., 2022). Two processes of within-island species diversification can
be hypothesized: (1) ex situ origination from adjacent areas
(e.g., Chiang & Schaal, 2006) and (2) in situ speciation within
the island (e.g., Cowie, 1995). The former is similar to the anagenetic
speciation process involving colonization of an island, whereas the
latter describes cladogenetic speciation within an island (Stuessy et
al., 2006). Emerson and Patino (2018) suggested the terms ”regional
allopatric” and ”regional sympatric speciation” as alternatives to
anagenetic and cladogenetic speciation, respectively. Regardless of
whether the speciation mode is ex situ origin or in situ ,
island species live and evolve within a confined area, which increases
contact opportunities and the possibility of hybridization and
introgression. These interbreeding opportunities accelerate evolution
within the island and, in turn, facilitate in situdiversification.
Adaptive introgression may lead to the introduction of novel genetic
combinations that contribute to adaptive traits and the emergence of new
species (Harrison & Larson, 2014). The transfer of these advantageous
genetic elements across species boundaries can promote the emergence of
individuals with wide adaptability to the island’s varying ecological
niches (Grant & Grant, 2019). The environmental heterogeneity of the
island provides numerous selection pressures that drive the evolution of
these hybrid populations. As a result, the genetic swarm formed through
hybridization enhances the resilience and adaptability of island
species, enabling them to persist and diverge rapidly in isolated
habitats (Grant & Grant, 2019). In some cases, hybrid speciation may
occur, with the hybrid swarm evolving into a distinct and reproductively
isolated species adapted to the island’s specific conditions (e.g.,
Argyranthemum [Asteraceae] on the Canary Island, Brochmann, Borgen,
& Stabbetorp, 2000)). Overall, the interplay between local adaptation
and adaptive introgression enriches the genetic diversity and ecological
complexity of island species.
Continental islands, such as Taiwan Island, repeatedly connected and
disconnected from the mainland due to sea level changes during glacial
oscillations (Lin, 1963; Yu, 2003). Continent-island connectivity leads
to the formation of new species from the continental ancestor and
prompts the colonization of islands and founder derivatives from the
continental progenitor, while within-island environmental heterogeneity
facilitates in situ diversification (Emerson & Patino, 2018).Scutellaria , commonly known as
skullcap, exhibits a high level of
endemism to Taiwan. Among the seven known species, five (S.
taiwanensis , S. hsiehii , S. tashiroi , S.
playfairii , and S. austrotaiwanensis ) are endemic, while the
other two (S. barbata and S. indica ) have wider
distributions across East, South, and Southeast Asia. Among the endemic
species, S. tashiroi is distributed in eastern Taiwan and the
Orchid Islet southeast of Taiwan, S. hsiehii is confined to
west-central Taiwan, and S. taiwanensis , S.
austrotaiwanensis , and S. playfairii are mainly distributed in
the south. On the basis of three chloroplast DNA fragments and two
low-copy nuclear genes, Chiang, Huang, and Liao (2012) proposed that
endemic S. tashiroi , S. playfairii , and S.
austrotaiwanensis descended from S. indica after colonizing
Taiwan and formed the ”indica group”. These three Taiwan-endemic
species are thus cladogenetic or regional sympatric species. By
contrast, S. taiwanensis and S. barbata (including its
synonym S. taipeiensis (Chao et al., 2020)) colonized Taiwan
independently during the Middle Pleistocene, i.e., 0.4 Mya (Chiang,
Huang, & Liao, 2012), and are so-called anagenetic or regional
allopatric species. The multiple colonization events suggest a
combination of in situ speciation and ex situ origin of
Taiwan’s Scutellaria species.
The demographic history of Scutellaria on Taiwan Island reveals
frequent southward and northward dispersal and vicariance events
(Chiang, Huang, & Liao, 2012), and their historical sympatric
distribution has allowed interbreeding (Huang et al., 2017). Their
morphological similarities (Chao et al., 2020; Hsieh, 2013; Hsieh &
Huang, 1995, 1997) and relatively short speciation history (Chiang,
Huang, & Liao, 2012) suggest that this group of species has only
recently completed or is still undergoing the speciation process. Their
adaptation to diverse environments and repeated secondary contacts
allowing hybridization and introgression have likely played critical
roles in maintaining their species and genetic diversities. To better
understand how island-endemic species adapt to their surroundings, we
performed multilocus genome scanning using the chromosome-scale genome
of S. baicalensis as a reference to examine the evolutionary
relationships among Scutellaria species in Taiwan. We analyzed
the occurrence and significance of introgression events between closely
related island species and explored the potential role of these events
in promoting hybrid speciation. Additionally, we investigated the impact
of local adaptation on the maintenance of species boundaries between
rapidly diverging island species.