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.