Integrating genomics and biogeography to unravel the origin of a mountain biota: The case of a reptile endemicity hotspot in Arabia

Advances in genomics have greatly enhanced our understanding of mountain biodiversity, providing new insights into the complex and dynamic mechanisms that drive the formation of mountain biotas. These span from broad biogeographic patterns to population dynamics and adaptations to these environments. However, significant challenges remain in integrating large-scale and fine-scale findings to develop a comprehensive understanding of mountain biodiversity. One significant challenge is the lack of genomic data, particularly in historically understudied arid regions where reptiles are a particularly diverse vertebrate group. In the present study, we assembled a de novo genome-wide SNP dataset for the complete endemic reptile fauna of a mountain range (19 described species with more than 600 specimens sequenced), and integrated state-of-the-art biogeographic analyses at the population, species and community level. Thus, we provide for the first time a holistic integration of how a whole endemic reptile community has originated, diversified and dispersed through a mountain system. Our results show that reptiles independently colonized the Hajar Mountains of southeastern Arabia 11 times. After colonization, species delimitation methods suggest high levels of within-mountain diversification, supporting up to 49 putative species. This diversity is strongly structured following local topography, with the highest peaks acting as a broad barrier to gene flow among the entire community. Surprisingly, orogenic events do not seem key drivers of the biogeographic history of reptiles in this system. Instead, past climatic events seem to have had a major role in this community assemblage. We observe an increase of vicariant events from Late Pliocene onwards, coinciding with an unstable climatic period of rapid shifts between hyper-arid and semiarid conditions that led to the ongoing desertification of Arabia. We conclude that paleoclimate, and particularly extreme aridification, acted as a main driver of diversification in arid mountain systems which is tangled with the generation of highly adapted endemicity. Overall, our study does not only provide a valuable contribution to understanding the evolution of mountain biodiversity, but also offers a flexible and scalable approach that can be reproduced into any taxonomic group and at any discrete environment.Funding provided by: MCIN/AEI/10.13039/501100011033*Crossref Funder Registry ID: Award Number: PGC2018-098290-B-I00 (MCIU/AEI/FEDER, UE)Funding provided by: ERDF, A way of making Europe*Crossref Funder Registry ID: Award Number: PID2021-128901NB-I00Funding provided by: Ministerio de Ciencia, Innovación y UniversidadesCrossref Funder Registry ID: http://dx.doi.org/10.13039/100014440Award Number: FPU18/04742Funding provided by: 'la Caixa' FoundationCrossref Funder Registry ID: http://dx.doi.org/10.13039/100010434Award Number: LCF/BQ/DR20/11790007Funding provided by: MCIN/AEI/10.13039/501100011033*Crossref Funder Registry ID: Award Number: FJC2021-046832-IFunding provided by: Fundação para a Ciência e a TecnologiaCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001871Award Number: DL57/2016/CP1440/CT0008Funding provided by: Czech Science FoundationCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001824Award Number: 22-12757SFunding provided by: Charles University Research Centre*Crossref Funder Registry ID: Award Number: 204069Funding provided by: Ministerio de Ciencia, Innovación y UniversidadesCrossref Funder Registry ID: http://dx.doi.org/10.13039/100014440Award Number: PRE2019-088729Raw ddRADseq demultiplexed reads are available and can be processed with ipyrad (https://ipyrad.readthedocs.io/). Supplementary figures, supplementary tables datasets and tree files are uploaded as separate files