Deforestation-induced Hybridization in Philippine Frogs Creates a Distinct Phenotype With an Inviable Genotype

Abstract

Hybridization plays a major role in the evolutionary history of many taxa and can generate confounding patterns affecting many downstream applications. In this study, we empirically demonstrate how hybridization obfuscates phylogenetic inference (via the artefactual branch effect), species boundaries, and taxonomy in an adaptive radiation of frogs. Philippine narrow-mouthed frogs of the genus Kaloula exhibit a wide range of phenotypic and ecological adaptations but their evolutionary history and taxonomy remain poorly understood. In particular, the Kaloula conjuncta complex contains numerous subspecies with unresolved taxonomic boundaries and unclear evolutionary relationships. Within this complex, Kaloula conjuncta stickeli, until now was considered a rare, enigmatic, and phenotypically distinct subspecies that had not been encountered since its original description nearly 80 years ago. Here, we show that K. c. stickeli shares alleles with K. conjuncta meridionalis and another species outside the conjuncta group, K. picta. Using target-capture sequencing and a robust analytical framework, we show that despite having a unique phenotype, K. c. stickeli is likely an inviable F1 hybrid between K. c. meridionalis and K. picta and thus, does not warrant taxonomic recognition. Our results show how industry-standard approaches in systematic inference and integrative taxonomy—morphological, phylogenomic, clustering, and distance-based methods—can generate misleading results for identifying and understanding affinities of hybrids. In contrast, we demonstrate how network multispecies coalescent and population genetic approaches are more effective at accurately inferring reticulated evolutionary history. We also propose a rare phenomenon of deforestation-induced hybridization, which could have important consequences in light of large-scale Southeast Asian forest destruction.