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A Tibetan Cradle of Evolution - in-situ speciation and Out-of-Tibet radiations in passerine model species

Subject Area Evolution, Anthropology
Term from 2012 to 2022
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 224578574
 
Final Report Year 2022

Final Report Abstract

The Qinghai-Tibet Plateau (QTP) is the World’s highest and largest plateau and along its margins it is flanked by four major biodiversity hotspots: the Central Asian Mountains in the West, the Himalayas and the Indo-Burmese Mountains in the South and the Hengduanshan in the East. In the first funding phase, this project was part of an interdisciplinary DFG Research Cluster PAK 807 (2013-2017) that was dedicated to the analysis of evolutionary and biogeographic history of alpine animals and plants using deep time-calibrated phylogenies. The basic a-priori hypothesis was a Tibetan origin of cold-adapted Eurasian faunal and floral elements (e.g. the Pleistocene and Holocene mammals) followed by several northward out-of-Tibet movements. However, for a speciose group of passerine birds, the Passeroidea (data set of 660 taxa) we found that faunal interchange between the QTP and adjacent regions was not a one-way street. We identified five passeroid clades that represent independent Eurasian radiations with an onset of diversification in the mid to late Miocene. Three groups showed a pattern of in-situ diversification in the QTP region with one or two out-of-Tibet/Himalayas dispersal events during the Pleistocene, whereas the two other groups originated and diversified in ancestral areas beyond the QTP range and showed recent into-Tibet dispersal events. Such bidirectional colonization pathways into and out-of the QTP are in good accordance with patterns of biogeographic history reconstructed for alpine plants (such as Saxifragaceae) by partners from DFG PAK 807. Furthermore, we found evidence of rather ancient emergence of QTP endemics from the high alpine plateau region with oldest species-level lineages dating back to the Oligocene-Miocene boundary (Prezvalski’s Finch, montypic family Urocynchramidae). Remarkably, net-diversification rates were not associated with mountain clades of Passeroidea which is partly in accordance with a recent paradigm shift that „young“ lineage splits (from the Miocene onwards) cannot be linked to the QTP uplift, because the plateau region must have reached its current mean elevation already within the course of the Eocene. In the second funding phase, we generated genome-wide SNP data sets to analyse intra- and interspecific patterns of divergence and admixture at shallower levels of divergence. Using optimized wet-lab protocols for mitogenome sequencing and for ddRAD seq analysis we were able to generate novel sequence data from about 60-year-old museum specimens, including a rare endemic from Central Asia (Afghan Snowfinch). The more recent speciation processes in terminal clades of the passeroid tree were associated with regional and global climate cooling towards the end of the Pliocene and typically shaped two major phylogeographic patterns. High-alpine specialists underwent further in-situ speciation on the QTP (center of origin and diversification) with up to six QTP endemics sharing a large range of sympatry on the plateau (snowfinches, Montifringilla and allies). As terminal colonization events, trans- and intercontinental dispersal occured in two QTP clades northeastwards into the Nearctic (rosy finches, Leucosticte) and to the western Palearctic (Montifringilla). Westward out-of-QTP dispersal in the White-winged Snowfinch (Montifringilla nivalis) was associated with strong genetic divergence between an eastern Asian lineage (northern QTP margin + Caucasus) and a western lineage. Analysis of a genome-wide SNP data set even allowed for distinction of two European genetic clusters (Alps and Cantabrian Mountains) that diverged in the mid to late Pleistocene. On the other hand, forest-dwelling passerine birds show a typical phylogeographic pattern of circum-Tibetan vicariance with at least one Sinohimalayan clade opposed to a northern Palearctic counterpart. Areas of range overlap, hybridization and gene flow between adjacent genetically distinctive taxa were identified in the central and eastern Palearctic and in the central and western Himalayas. The result of lineage divergence during the same evolutionary time period can be strikingly different among closest relatives, e.g. in Periparus tits. Secondary contact among eastern and western counterparts in central Nepal has resulted in A) a narrow hybrid zone including directional gene flow between Coal Tits and Spot-winged Tits (P. a. aemodius, P. a. melanolophus), and B) regional sympatry under absence of gene flow between Rufous-backed Tits and Rufous-vented Tits (P. rufonuchalis, P. rubidiventris). Divergence of territoral songs is suggested to be a major premating barrier in the latter species pair. Out-of-QTP dispersal in these tits towards the Western Palearctic was associated with the formation of further zones of intergradation and gene flow in China and in Central Europe. Future studies on whole-genome data might provide further insight on the role of functional candidate genes in adaptive radiations (e.g. adaptation to extreme alpine environments) or divergence of behavioral traits (e.g. vocalizations).

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