Ancient allopatry and ecological divergence act together to promote plant diversity in mountainous regions: evidence from comparative phylogeography of two genera in the Sino-Himalayan region

Abstract

Background: How geographical isolation and ecological divergence act together to promote plant diversity in mountainous regions remains largely unknown. In this study, we chose two small genera distributed in the Sino-Himalayan region, Megacodonand Beesia, which both exhibit a fragmented distribution pattern and are found across a wide range of altitudes. By summarizing their common patterns of speciation and/or divergence processes, we aim to understand how environmental changes accelerated lineage diversification in the Sino-Himalayan region through ancient allopatry and ecological divergence. Results: Using ddRAD-seq, chloroplast genome sequences, and specific molecular markers, we studied the phylogenetic relationships, population structure, and historical biogeography of Beesia and Megacodon. Both genera began to diverge from the late Miocene onwards, with ancient allopatry at lower altitudes formed narrow-range species or relict populations. Mantel tests between genetic distance and climatic, elevational, or geographic distance revealed an isolation-by-distance pattern in Beesia and Megacodon stylophorus. Megacodon showed two clades occupying entirely different altitudinal ranges, whereas Beesia calthifoliaexhibited a genetic divergence pattern along an altitude gradient. To investigate adaptive divergence along an altitudinal gradient, we used morphological measurements and found different elevational groups in Beesia calthifolia had distinct leaf shapes. Conclusions: The regional disjunctions of plant groups in the Sino-Himalayan region are drastic and closely related to several biogeographic boundaries. As a consequence of major geological and climate change, ecological divergence when different altitudes are colonized often happens simultaneously within plant groups. Although the relative contributions of geographical isolation and parapatric ecological divergence are different among different plant taxa, a combined effect of these two factors is a common phenomenon in the process of heterogenization of the Sino-Himalayan region.