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 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 deep lineages. This diversity is strongly structured following local topography, with the highest peaks acting as a broad barrier to gene flow among the entire community. Interestingly, 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.

Clinging on the brink: Whole genomes reveal human-induced population declines and severe inbreeding in the Critically Endangered Emirati Leaf-toed Gecko (Asaccus caudivolvulus).

Human-mediated habitat destruction has had a profound impact on increased species extinction rates and population declines worldwide. The coastal development in the United Arab Emirates (UAE) over the last two decades, serves as an example of how habitat transformation can alter the landscape of a country in just a few years. Here, we study the genomic implications of habitat transformation in the Critically Endangered Emirati Leaf-toed Gecko (Asaccus caudivolvulus), the only endemic vertebrate of the UAE. We generate a high-quality reference genome for this gecko, representing the first reference genome for the family Phyllodactylidae, and produce whole-genome resequencing data for 23 specimens from 10 different species of leaf-toed geckos. Our results show that A. caudivolvulus has consistently lower genetic diversity than any other Arabian species of Asaccus, suggesting a history of ancient population declines. However, high levels of recent inbreeding are recorded among populations in heavily developed areas, with a more than 50% increase in long runs of homozygosity within a 9-year period. Moreover, results suggest that this species does not effectively purge deleterious mutations, hence making it more vulnerable to future stochastic threats. Overall, results show that A. caudivolvulus is in urgent need of protection, and habitat preservation must be warranted to ensure the species' survival.

Hidden in the sand: Phylogenomics unravel an unexpected evolutionary history for the desert-adapted vipers of the genus Cerastes.

The desert vipers of the genus Cerastes are a small clade of medically important venomous snakes within the family Viperidae. According to published morphological and molecular studies, the group is comprised by four species: two morphologically similar and phylogenetically sister taxa, the African horned viper (Cerastes cerastes) and the Arabian horned viper (Cerastes gasperettii); a more distantly related species, the Saharan sand viper (Cerastes vipera), and the enigmatic Böhme's sand viper (Cerastes boehmei), only known from a single specimen in captivity allegedly captured in Central Tunisia. In this study, we sequenced one mitochondrial marker (COI) as well as genome-wide data (ddRAD sequencing) from 28 and 41 samples, respectively, covering the entire distribution range of the genus to explore the population genomics, phylogenomic relationships and introgression patterns within the genus Cerastes. Additionally, and to provide insights into the mode of diversification of the group, we carried out niche overlap analyses considering climatic and habitat variables. Both nuclear phylogenomic reconstructions and population structure analyses have unveiled an unexpected evolutionary history for the genus Cerastes, which sharply contradicts the morphological similarities and previously published mitochondrial approaches. Cerastes cerastes and C. vipera are recovered as sister taxa whilst C. gasperettii is a sister taxon to the clade formed by these two species. We found a relatively high niche overlap (OI > 0.7) in both climatic and habitat variables between C. cerastes and C. vipera, contradicting a potential scenario of sympatric speciation. These results are in line with the introgression found between the northwestern African populations of C. cerastes and C. vipera. Finally, our genomic data confirms the existence of a lineage of C. cerastes in Arabia. All these results highlight the importance of genome-wide data over few genetic markers to study the evolutionary history of species.

Species boundaries to the limit: Integrating species delimitation methods is critical to avoid taxonomic inflation in the case of the Hajar banded ground gecko (Trachydactylus hajarensis).

With the advent of molecular phylogenetics and the implementation of Multispecies Coalescent-based (MSC) species delimitation methods (SDM), the number of taxonomic studies unveiling and describing cryptic sibling species has greatly increased. However, speciation between early divergent lineages is often defined without evaluating population structure or gene flow, which can lead to false claims of species status and, subsequently, taxonomic inflation. In this study, we focus on the intriguing case of the Arabian gecko Trachydactylus hajarensis (Squamata: Gekkonidae). We generated mitochondrial data (12S rDNA) and genome-wide SNP data (ddRADseq) for 52 specimens to determine phylogenomic relationships, population structure and genetic diversity within this species. Then, we applied a set of different SDMs to evaluate several competing species hypotheses through the MSC. Results show that T. hajarensis is comprised by three well-defined population lineages, two of them in the Hajar Mountains of eastern Arabia, and one in Masirah Island, on the southeastern coast of Oman. Strong mito-nuclear discordances were found between populations inhabiting the Hajar Mountains, but we did not find evidence of current gene flow between them. Surprisingly, discordances in species tree topology were found when different downsampled datasets were used, and especially when linking population sizes, a commonly implemented feature in species tree reconstruction with genomic data. Different SDMs yielded different results, supporting from four species within the group, to T. hajarensis being a single species. With such contrasting results we suggest caution before splitting T. hajarensis. Overall, this study highlights the importance of sample and prior choice and the integration of several SDMs to not incur into taxonomic inflation, providing a set of already available tools to assess population structure, genetic diversity, and SDMs before describing new species.

Integrative systematic revision of the Montseny brook newt (Calotriton arnoldi), with the description of a new subspecies.

The Montseny brook newt (Calotriton arnoldi), a glacial relict endemic to a small, isolated massif in northeast Spain, is considered the only Critically Endangered urodele in Europe. Its restricted range is divided by a deep valley that acts as an impassable barrier to dispersal, separating two isolated metapopulations (Western and Eastern) that correspond to independent lineages with different evolutionary trajectories, based on genetic and genomic data. Here, we address the ecological differentiation between lineages and discuss its potential effect on the phenotypic distinctness of each lineage. Based on multiple lines of evidence, we formally describe the Western Montseny brook newt as a new subspecies: Calotriton arnoldi laietanus ssp. nov. Finally, our study underscores the importance of considering taxonomic progress in the conservation policies of endangered species, ensuring appropriate management and protection of the newly described taxa.

Genomic insights into the Montseny brook newt (Calotriton arnoldi), a Critically Endangered glacial relict.

The Montseny brook newt (Calotriton arnoldi), considered the most endangered amphibian in Europe, is a relict salamandrid species endemic to a small massif located in northeastern Spain. Although conservation efforts should always be guided by genomic studies, those are yet scarce among urodeles, hampered by the extreme sizes of their genomes. Here, we present the third available genome assembly for the order Caudata, and the first genomic study of the species and its sister taxon, the Pyrenean brook newt (Calotriton asper), combining whole-genome and ddRADseq data. Our results reveal significant demographic oscillations which accurately mirrored Europe's climatic history. Although severe bottlenecks have led to depauperate genomic diversity and long runs of homozygosity along a gigantic genome, inbreeding might have been avoided by assortative mating strategies. Other life history traits, however, seem to have been less advantageous, and the lack of land dispersal has driven to exceptional levels of population fragmentation.

Evolution along allometric lines of least resistance: morphological differentiation in Pristurus geckos.

Species living in distinct habitats often experience unique ecological selective pressures, which can drive phenotypic divergence. However, how ecophenotypic patterns are affected by allometric trends and trait integration levels is less well understood. Here we evaluate the role of allometry in shaping body size and body form diversity in Pristurus geckos utilizing differing habitats. We found that patterns of allometry and integration in body form were distinct in species with different habitat preferences, with ground-dwelling Pristurus displaying the most divergent allometric trend and high levels of integration. There was also strong concordance between intraspecific allometry across individuals and evolutionary allometry among species, revealing that differences in body form among individuals were predictive of evolutionary changes across the phylogeny at macroevolutionary scales. This suggested that phenotypic evolution occurred along allometric lines of least resistance, with allometric trajectories imposing a strong influence on the magnitude and direction of size and shape changes across the phylogeny. When viewed in phylomorphospace, the largest rock-dwelling species were most similar to the smallest ground-dwelling species, and vice versa. Thus, in Pristurus, phenotypic evolution along the differing habitat-based allometric trajectories resulted in similar body forms at differing body sizes in distinct ecological habitats.

Genomics reveals introgression and purging of deleterious mutations in the Arabian leopard (Panthera pardus nimr).

In endangered species, low-genetic variation and inbreeding result from recent population declines. Genetic screenings in endangered populations help to assess their vulnerability to extinction and to create informed management actions toward their conservation efforts. The leopard, Panthera pardus, is a highly generalist predator with currently eight different subspecies. Yet, genomic data are still lacking for the Critically Endangered Arabian leopard (P. p. nimr). Here, we sequenced the whole genome of two Arabian leopards and assembled the most complete genomic dataset for leopards to date. Our phylogenomic analyses show that leopards are divided into two deeply divergent clades: the African and the Asian. Conservation genomic analyses indicate a prolonged population decline, which has led to an increase in inbreeding and runs of homozygosity, with consequent purging of deleterious mutations in both Arabian individuals. Our study represents the first attempt to genetically inform captive breeding programmes for this Critically Endangered subspecies.