Application to other species
Can this strategy be applied to document homoploid hybrid speciation in other systems (Figure 1)? The short answer is “yes”, with an additional plant example (Wang, Kang et al., 2022), as well as examples from charismatic megafauna including bears (Zou et al. 2022) and primates (Wu et al., 2023; Zhang et al., 2023). The second plant example also comes from the Betulaceae, but involves hybridization between two different genera of trees and shrubs, Ostrya and Carpinus(Wang, Kang et al., 2022), which diverged 23-33 mya. Hybridization between them gave rise to a new lineage (Carpinussection Distegocarpus ), which has since diversified into three species. Diversification following hybridization does not seem to be uncommon, especially in adaptive radiations (e.g., Meier et al., 2017; Owens et al., 2023; Stull et al., 2023; Wogan et al., 2023). Phylogenomic analyses indicate that section Distegocarpus is ancient as well, with an origin (17–26 mya) fairly close in time to the divergence of the parental lineages. Searches for positively selected and highly differentiated genes using the pipeline of Wang et al. (2021) identified genes likely involved in habitat and flowering time barriers from the alternate parental lineages, thereby tentatively linking hybridization to the development of reproductive barriers. In addition, because homoploid hybrid speciation was so ancient in this case, the authors validated their results with a parallel pipeline based on indels, which are expected to be less vulnerable to homoplasy than nucleotide substitutions (Rokas & Holland, 2000).
In bears, phylogenomic analyses showed that Asiatic black bears arose via hybridization between the ancestor of polar/brown/American black bears and the ancestor of sun/sloth bears (Zou et al. 2022). Simulations of demographic further suggested that the parental lineages diverged ∼5.91 mya, with the origin of Asiatic black bears occurring just 0.25 mya later. Using the Wang et al. (2021) pipeline for detecting positively selected genes, Zou et al. (2022) identified candidate genes underlying the intermediate body size of Asiatic black bears. As in the previous two plant examples, candidate genes were inherited from the alternate parental lineages and may contribute to assortative mating in bears. Such alternate inheritance patterns were also observed for positively selected genes underlying reproductive processes, including male fertility, fertilization, and sperm development. Zou et al. (2022) argue that these may represent Bateson-Dobzhansky-Muller (BDM) incompatibilities, but this hypothesis remains to be confirmed by functional analyses.
The situation in primates is surprisingly similar to that found for bears. In macaques, which are the most widespread primates after humans, it was found that ancient hybridization between the sinica andsilenus groups in Southeast Asia gave rise to thefascicularis group, which includes four closely related species. Similar to bears, the fascicularis lineage originated shortly after (∼0.35 mya) the divergence of the parental lineages (~3.86 mya). Positively selected genes underlying a mosaic of parental traits, including sexually selected traits, were found to be inherited from the different parental lineages. The authors argue that such a distinct mix of sexual phenotypes could result in assortative mating, thereby enabling the establishment of the new hybrid lineage. Likewise, phylogenomic analyses of snub-nosed monkeys (Rhinopithecus ) from China revealed that the gray snub-nosed monkey (R. brelichi ) originated by hybridization between the golden snub-nosed monkey and the ancestor of black and black-white snub-nosed monkeys (Wu et al. 2023). As with the macaques and bears, hybrid origin (∼1.87 mya) was close in time to parental lineage divergence (1.98 mya). The distinct coat coloration of the hybrid species is thought to contribute premating isolation with its parental species. Using the Wang et al. (2021) pipeline, candidate genes underlying coat coloration were found to be derived from alternate parental lineages, providing a link between hybridization and premating isolation in this system as well.
Together these five studies highlight the power of the Wang et al. (2021) approach for documenting homoploid hybrid speciation (Figure 1). Their strategy can be applied to any system, such as putative cases of homoploid hybrid speciation recently published in this journal (Cuevas et al., 2021; Li et al., 2021; Popoli Yazdi et al., 2022). However, keep in mind that the strength of the resulting inferences will depend on the extent of background information about the kinds and importance of different reproductive barriers in a given system and the genes that underlie them. For example, the case for homoploid hybrid speciation ofOstryopsis intermedia is especially strong because state of the art methods were used to identify and order the reproductive barriers isolating it from its parental species and to functionally validate key genes underlying the reproductive barriers. In the other four papers, while reasonable inferences were made about likely reproductive barriers and the underlying genes, the level of proof is lower.