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.