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.