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 genera comprising a small number of species distributed in the Sino-Himalayan region, Megacodon (Gentianaceae)...

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Main Authors: Junchu Peng, Xiangguang Ma, Hang Sun
Format: Article
Language:English
Published: BMC 2023-11-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04593-1
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author Junchu Peng
Xiangguang Ma
Hang Sun
author_facet Junchu Peng
Xiangguang Ma
Hang Sun
author_sort Junchu Peng
collection DOAJ
description 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 genera comprising a small number of species distributed in the Sino-Himalayan region, Megacodon (Gentianaceae) and Beesia (Ranunculaceae), which both exhibit a fragmented distribution pattern and are found across a wide range of elevations. 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 elevations 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 calthifolia exhibited a genetic divergence pattern along an elevation gradient. Furthermore, we conducted morphological measurements on Beesia calthifolia and found that different elevational groups 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 elevations are colonized often happens simultaneously within plant groups. Although habitat fragmentation and parapatric ecological divergence each spur speciation to different extents, a combined effect of these two factors is a common phenomenon in the Sino-Himalayan region.
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spelling doaj.art-1c09e7f29ec340fcad7400506ec5771d2023-11-19T12:52:20ZengBMCBMC Plant Biology1471-22292023-11-0123111710.1186/s12870-023-04593-1Ancient allopatry and ecological divergence act together to promote plant diversity in mountainous regions: evidence from comparative phylogeography of two genera in the Sino-Himalayan regionJunchu Peng0Xiangguang Ma1Hang Sun2CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of SciencesCAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of SciencesCAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of SciencesAbstract 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 genera comprising a small number of species distributed in the Sino-Himalayan region, Megacodon (Gentianaceae) and Beesia (Ranunculaceae), which both exhibit a fragmented distribution pattern and are found across a wide range of elevations. 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 elevations 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 calthifolia exhibited a genetic divergence pattern along an elevation gradient. Furthermore, we conducted morphological measurements on Beesia calthifolia and found that different elevational groups 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 elevations are colonized often happens simultaneously within plant groups. Although habitat fragmentation and parapatric ecological divergence each spur speciation to different extents, a combined effect of these two factors is a common phenomenon in the Sino-Himalayan region.https://doi.org/10.1186/s12870-023-04593-1Comparative phylogeographyBeesiaMegacodonSino-HimalayanEcological divergenceHabitat fragmentation
spellingShingle Junchu Peng
Xiangguang Ma
Hang Sun
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
BMC Plant Biology
Comparative phylogeography
Beesia
Megacodon
Sino-Himalayan
Ecological divergence
Habitat fragmentation
title 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
title_full 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
title_fullStr 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
title_full_unstemmed 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
title_short 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
title_sort 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
topic Comparative phylogeography
Beesia
Megacodon
Sino-Himalayan
Ecological divergence
Habitat fragmentation
url https://doi.org/10.1186/s12870-023-04593-1
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