The origin of a mountain biota: hyper-aridity shaped reptile diversity in an Arabian biodiversity hotspot

Abstract

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 include from broad biogeographic patterns, to population dynamics and adaptations to these environments. However, significant challenges remain in integrating these 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. We generated de novo genome-wide SNP data for more than 600 specimens and integrated state-of-the-art biogeographic analyses at the community, species and population level. We, thus, provide for the first time, a holistic integration of how a whole endemic reptile community has originated, diversified and dispersed through a mountain range. Our results show that reptiles independently colonized the Hajar Mountains of eastern 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 to rise as key drivers of the biogeographic history of reptiles in this system. However, paleoclimate seems 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 to 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. Our study provides a valuable contribution to understanding the evolution of mountain biodiversity and the role of environmental factors in shaping the distribution and diversity of reptiles in arid regions.