Reticulate evolution involves hybrid speciation events that combine two species to produce a third one with or without polyploidization, introgression and horizontal gene transfer between different species (Fig. 1A) (Linder et al., 2004). This is in contrast to the Darwin sketch of a bifurcating tree (Fig. 1B) (Trier et al., 2014; Wang et al., 2021), which is assumed to originate mainly through allopatric speciation, especially in mountainous ecosystems (Mayr, 1976). It is challenging to infer credible ancient reticulate evolutionary patterns and so build a connection between hybridization and species diversification. In this issue, Yang et al. (2023) detect widespread reticulate evolution in the species radiation of the genus Buddleja (Scrophulariaceae) in the Sino-Himalayan region, a biodiversity hotspot with numerous endemics in the Northern Hemisphere (Wu et al., 2022). They further infer that many reticulations involved allopolyploid speciation events arising from interspecific hybridization and polyploidization, based on multiple lines of evidence from phylogenomic reconstruction, reticulate evolution analyses, genetic composition and ploidy level. The many hybrid speciation events inferred in this study highlight the critical role of reticulate evolution in generating current biological diversity. In addition to allopolyploidizations, they also identify multiple autopolyploidizations that involve only one species without interspecific hybridization. Based on the maternally inherited plastome phylogeny, most hybridization and polyploidization events were dated to within the last three million years, likely suggesting that their origins were triggered by the Quaternary climatic oscillations in the genus in the Sino-Himalayan region. This finding updates the prior paradigm that mountain uplifts since the Oligocene and the accompanying climate changes contributed to species diversity in these mountainous ecosystems mainly through allopatric isolations (e.g. Ding et al., 2020).
(A) Network representation of phylogeny including both vertical inheritance and lateral genetic exchange (from Dagan and Martin, 2009). (B) Darwin’s tree, showing bifurcating speciation events. This pattern is often attributed to an allopatric mode of speciation, in which geological and climactic change fragment a population into geographically isolated sub-populations that over time lose the capacity to interbreed and so become new species.
Hybridizations between closely related species have previously been found to be widespread for species-rich genera distributed in the Sino-Himalayan region (Yang et al., 2019; Wu et al., 2022). Current hybridization events produce hybrid populations that have not yet developed reproductive isolation (RI) as an independently evolving lineage (Liu, 2016). However, ancient hybridizations may have produced distinct species with RI through inheriting alternative RI alleles from both parents (Wang et al., 2021), developing specific genomic or chromosomal changes (Rieseberg and Willis, 2007) or undergoing polyploidization through merging the chromosomes of both parents (Abbott et al., 2013). Homoploid hybrid species were found for many groups in this region (Wang et al., 2021; Wu et al., 2022; Ma et al., 2023). However, allopolyploid species were rarely reported and confirmed in this region (Nie et al., 2005; Wu et al., 2022). The study of Yang et al. (2023) used the reticulate analyses and multiple approaches to show that hybrid species with or without polyploidization prevail in the genus Buddleja, highlighting again the important roles of both hybridization and polyploidization in creating species diversity in the Sino-Himalayan region.
Sympatric speciation without geographical isolation, comprising ecological divergence, hybrid speciation and polyploidization, is suggested to play a key role in species diversification in plants (Wu et al., 2022). This is especially true for polyploidization. For example, polyploidizations or whole-genome duplications were found to have occurred across the diversification of the flowering plant lineage (Cai et al., 2018; One Thousand Transcriptomes Initiative, 2019). However, it is difficult to discern whether a particular clade or species originated through autopolyploidization or allopolyploidization. In particular, except for counting chromosomes of the samples, many new methods in the genomic era were developed to infer polyploidization events, including Ks-based methods, ancestral chromosome counts, gene tree-based methods and synteny-based methods. Among these methods, the synteny-based method is considered the most reliable for detecting polyploidizations (Cai et al., 2018). The chromosome-counting method is less powerful for detecting ancient polyploidization events (Cai et al., 2018) except in the scenario where the ancestors with low chromosome numbers are still present. This is true for the genus Buddleja (Yang et al., 2023) and therefore the authors adopted a simpler method that measured the DNA contents (corresponding to the ploidy level) through flow cytometry to determine the ploidy levels of the sampled materials. Yang et al. (2023) identified 15 of the 27 sampled Asian Buddleja species as polyploids using this method. The high proportion of polyploid species obviously suggests that polyploidization should have contributed greatly to the species diversification of this genus in the Sino-Himalayan region, in contrast to the early predication that the species diversification in this region mainly occurs at the diploid level (Nie et al., 2005). In fact, the critical role of polyploidization in species diversification in this region as well as the other regions of the world has long been underestimated (Mao et al., 2021).
To conclude, Yang et al. (2023) presented a particular case study in which both hybridization and polyploidization contributed to species diversification in plants in the Sino-Himalayan region based on well-constructed evolutionary history through reticulate analyses and multiple approaches. Their results further show that the Quaternary climatic oscillations, which possibly led to range changes following hybridizations between previously isolated species, have greatly contributed to a pattern of species diversification through both allopatric and (sympatric) hybrid speciation (Fig. 1B). Such net-like phylogenies (Dagan and Martin, 2009) have rarely been shown, and examples supported by solid genomic phylogenies and confirmed ploidy levels are especially rare (Wang et al., 2023). In the future, more case studies should be encouraged to investigate reticulate evolution in plants, in this region and elsewhere, as done by Yang et al. (2023). It is especially important to understand how sympatric hybridization and allopatric isolation, two ‘opposing’ mechanisms, in fact interact or reinforce each other to rapidly create new independently evolving lineages.
