Multidimensional divergence supports parapatric speciation along an elevational gradient in ground-dwelling frogs on an oceanic island

Abstract

Geographic isolation is a major driver of lineage divergence. However, strong ecological selection can promote reproductive isolation despite opportunities for gene flow in geographically continuous landscapes such as mountains. Here, we test whether ecological divergence across elevational gradients can promote speciation within a single mountain range. Integrating phylogenomic (ddRAD), morphological, and bioacoustic data, we test predictions of elevation-mediated parapatric speciation in Platymantis (Lahatnanguri) ground-dwelling frogs on Mindanao Island, Philippines. Phylogenomic analyses recovered an endemic radiation across neighboring mountain ranges and revealed a hierarchical pattern of diversification among three monophyletic lineages, with deeper divergence separating the mountain lineages Highland 1 and Highland 2 and more recent divergence occurring within a single mountain range. This topology identified a morphologically and acoustically distinct low-elevation lineage (<1,400 m a.s.l.) as closely related to the high-elevation Highland 1 lineage (>1,400 m a.s.l.), providing a natural test of divergence along an elevational gradient. The parapatric Lowland and Highland 1 lineages appear to have diverged relatively recently, as reflected in their shallow genome-wide differentiation, yet exhibit pronounced morphological and acoustic divergence. Population genomic analyses further recover discrete genomic clusters and no evidence of contemporary hybridization between the parapatric lineages, indicating independent evolutionary trajectories despite geographic continuity. Together, these findings are consistent with parapatric speciation along an elevational gradient and demonstrate how substantial phenotypic and reproductive-isolation divergence can accumulate despite limited genome-wide differentiation. More broadly, our results indicate that the exceptional biodiversity of oceanic archipelagos may arise not only from diversification among islands (and among mountains within islands) but also from lineage divergence along elevational gradients within mountains themselves. These empirical results support the biological plausibility of parapatric speciation within single mountain systems and highlight an underrecognized mechanism contributing to biodiversity in topographically complex oceanic archipelagos.