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

Pristurus guweirensis Haas, 1943 (Gekkota: Sphaerodactylidae): the most abundant and widely distributed species of Pristurus previously referred to as Pristurus sp. 1

Peer reviewe

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.This work was supported by grants PGC2018-098290-B-I00 (MCIU/AEI/FEDER, UE), Spain, PID2021-128901NB-I00 (MCIN/AEI/10.13039/501100011033 and by ERDF, A way of making Europe), Spain, and grant 2021-SGR-00751 from the Departament de Recerca i Universitats from the Generalitat de Catalunya, Spain to SC. GM-R is supported by an FPI grant from the Ministerio de Ciencia, Innovación y Universidades, Spain (PRE2019-088729), BB-C is supported by FPU grant from Ministerio de Ciencia, Innovación y Universidades, Spain (FPU18/04742), AT is supported by “la Caixa” doctoral fellowship program (LCF/BQ/DR20/11790007), HT-C is supported by a “Juan de la Cierva - Formación” postdoctoral fellowship (FJC2021-046832-I) funded by MCIN/AEI/10.13039/501100011033 and by the European Union NextGenerationEU/PRTR, GV-A was supported by the FCT (CEECIND/00937/2018) and recently by a Ramón y Cajal research grant (Ref. RYC-2019-026959-I/AEI/10.13039/501100011033), JŠ was supported by the Czech Science Foundation (GAČR) under grant number 22-12757S and by the Charles University Research Centre under grant number 204069 and FM-F and JCB are supported by FCT - Fundação para a Ciencia e Tecnologia de Portugal (DL57/2016/CP1440/CT0010, CEECINST/00014/2018/CP1512/CT0001, respectively).Peer reviewe

Desert lizard diversity worldwide: effects of environment, time, and evolutionary rate [Software]

[Aim] Biodiversity is not uniformly distributed across the Earth's surface, even among physiographically comparable biomes in different biogeographic regions. For lizards, the world's large desert regions are characterized by extreme heterogeneity in species richness, spanning some of the most species-rich (arid Australia) and species-poor (central Asia) biomes overall. Regional differences in species diversity may arise as a consequence of the interplay of several factors (e.g., evolutionary time, diversification rate, environment), but their relative importance for biogeographic patterns remains poorly known. Here we use distributional and phylogenetic data to assess the evolutionary and ecological drivers of large-scale variation in desert lizard diversity.[Location] Deserts worldwide.[Major taxa studied] Lizards (non-snake squamates).[Methods] We specifically test whether diversity patterns are best explained by differences in the ages of arid-adapted lineages (evolutionary time hypothesis), by regional variation in speciation rate, by geographic area of the arid systems, and by spatial variation related to the environment (climate, topography, and productivity).[Results] We found no effect of recent speciation rate and geographic area on differences in desert lizard diversity. We demonstrate that the extreme species richness of the Australian deserts cannot be explained by greater evolutionary time, because species began accumulating more recently there than in more species-poor arid regions. We found limited support for relationships between regional lizard richness and environmental variables, but these effects were inconsistent across deserts, showing a differential role of the environment in shaping the lizard diversity in different arid regions.[Main conclusions] Our results provide evidence against several classic hypotheses for interregional variation in species richness, but also highlight the complexity of processes underlying vertebrate community richness in the world's great arid systems.Peer reviewe

Desert lizard diversity worldwide: effects of environment, time, and evolutionary rate

This dataset is embargoed and will be released when the associated article is published.[Aim] Biodiversity is not uniformly distributed across the Earth's surface, even among physiographically comparable biomes in different biogeographic regions. For lizards, the world's large desert regions are characterized by extreme heterogeneity in species richness, spanning some of the most species-rich (arid Australia) and species-poor (central Asia) biomes overall. Regional differences in species diversity may arise as a consequence of the interplay of several factors (e.g., evolutionary time, diversification rate, environment), but their relative importance for biogeographic patterns remains poorly known. Here we use distributional and phylogenetic data to assess the evolutionary and ecological drivers of large-scale variation in desert lizard diversity.[Location] Deserts worldwide.[Major taxa studied] Lizards (non-snake squamates).[Methods] We specifically test whether diversity patterns are best explained by differences in the ages of arid-adapted lineages (evolutionary time hypothesis), by regional variation in speciation rate, by geographic area of the arid systems, and by spatial variation related to the environment (climate, topography, and productivity).[Results] We found no effect of recent speciation rate and geographic area on differences in desert lizard diversity. We demonstrate that the extreme species richness of the Australian deserts cannot be explained by greater evolutionary time, because species began accumulating more recently there than in more species-poor arid regions. We found limited support for relationships between regional lizard richness and environmental variables, but these effects were inconsistent across deserts, showing a differential role of the environment in shaping the lizard diversity in different arid regions.[Main conclusions] Our results provide evidence against several classic hypotheses for interregional variation in species richness, but also highlight the complexity of processes underlying vertebrate community richness in the world's great arid systems.Peer reviewe

Desert lizard diversity worldwide: effects of environment, time, and evolutionary rate [Dataset]

In this folder you can find the supplementary figures and tables of the paper.[Aim] Biodiversity is not uniformly distributed across the Earth's surface, even among physiographically comparable biomes in different biogeographic regions. For lizards, the world's large desert regions are characterized by extreme heterogeneity in species richness, spanning some of the most species-rich (arid Australia) and species-poor (central Asia) biomes overall. Regional differences in species diversity may arise as a consequence of the interplay of several factors (e.g., evolutionary time, diversification rate, environment), but their relative importance for biogeographic patterns remains poorly known. Here we use distributional and phylogenetic data to assess the evolutionary and ecological drivers of large-scale variation in desert lizard diversity.[Location] Deserts worldwide.[Major taxa studied] Lizards (non-snake squamates).[Methods] We specifically test whether diversity patterns are best explained by differences in the ages of arid-adapted lineages (evolutionary time hypothesis), by regional variation in speciation rate, by geographic area of the arid systems, and by spatial variation related to the environment (climate, topography, and productivity).[Results] We found no effect of recent speciation rate and geographic area on differences in desert lizard diversity. We demonstrate that the extreme species richness of the Australian deserts cannot be explained by greater evolutionary time, because species began accumulating more recently there than in more species-poor arid regions. We found limited support for relationships between regional lizard richness and environmental variables, but these effects were inconsistent across deserts, showing a differential role of the environment in shaping the lizard diversity in different arid regions.[Main conclusions] Our results provide evidence against several classic hypotheses for interregional variation in species richness, but also highlight the complexity of processes underlying vertebrate community richness in the world's great arid systems.Peer reviewe

Patterns and drivers of desert reptile diversity at different phylogenetic and spatial scales

Biodiversity patterns result from the interplay of evolutionary, ecological, and environmental processes. Investigating the drivers of such patterns is central to evolutionary biology, and it is further essential to understand how the undergoing global changes will shape the future of biodiversity. This thesis explores diversity patterns and their drivers at different taxonomic and spatial scales, using reptiles from arid regions as a model of study. Specifically, this thesis analyzes the ecomorphological diversity of the Afro-Arabian geckos of the genus Pristurus in the context of island colonization and habitat specialization, the biogeographic patterns of Afro-Arabian squamates in the light of the region's geologic and climatic history, and the differences in lizard richness among the greatest deserts of the world. General processes were identified as determinant for the evolution of arid reptiles, although the results also highlight the complexity and the system-specific nature of biodiversity patterns and their driversLos patrones de biodiversidad son el resultado de múltiples procesos evolutivos, ecológicos y ambientales. Estudiar las causas de dichos patrones es fundamental en biología evolutiva, y además es clave para entender el impacto de los presentes cambios globales en la biodiversidad. Esta tesis utiliza los reptiles de las zonas áridas para explorar patrones de diversidad y sus causas a distintas escalas taxonómicas y geográficas. Concretamente, se analizan la diversidad ecomorfológica de los geckos Pristurus en el contexto de la colonización de islas y la especialización de hábitat, los patrones biogeográficos de los reptiles de Afro-Arabia a la luz de la historia geológica y climática de la región, y las diferencias en diversidad de lagartos entre los grandes desiertos del mundo. Se identificaron procesos clave en la evolución de los reptiles de zonas áridas, pero los resultados también demuestran la complejidad de los patrones de diversidad y sus causas

Biogeographic and diversification patterns of squamate reptiles across North Africa and Arabia

Presentation given at the XXXVIII Annual Meeting of the Willi Hennig Society on May 26th-31st, 2019, in University of California at Berkeley.Desert areas comprise an important part of the world¿s land surface. In spite of their harsh conditions, deserts can harbor a high diversity of fauna and flora. This offers the opportunity of investigating how the geographic and climatic history of these areas have affected the evolutionary history of their biodiversity. In this study, we focus on some of the largest arid regions of the world, the north of Africa and the Arabian Peninsula, to study large-scale biogeographic and diversification patterns of squamate reptiles, one of the most successful groups inhabiting the deserts. Evolutionary history has been explored and discussed independently for several groups of reptiles from north Africa and the Arabian Peninsula, but a study integrating a large number of groups is still lacking. Here, we assemble a comprehensive dataset including most of the squamate genera present both in Africa and Arabia with the objective of investigating large-scale biogeographic and diversification patterns in a comparative framework. We reconstruct phylogenetic relationships among 550 species with 5 mitochondrial and 6 nuclear loci, and estimate divergence times with eleven calibration points, including fossils and biogeographic events. With this broad dataset, we are able to reconstruct and compare the evolutionary history of 22 genera of squamate reptiles across north Africa and Arabia. By applying statistical biogeographic models, we can associate diversification dynamics with paleogeographic events affecting these regions. As a result, we can describe the effect of the Afro-Arabian geologic and climatic history on the diversity and evolution of desert-dwelling squamates

Data from: Ecological specialization, rather than the island effect, explains morphological diversification in an ancient radiation of geckos

Island colonists are often assumed to experience higher levels of phenotypic diversification than continental taxa. However, empirical evidence shows that exceptions to this “island effect” do exist. Here, we tested this pattern using a thoroughly sampled continent-island system, the genus Pristurus, a group of sphaerodactylid geckos distributed across continental Arabia and Africa and the Socotra Archipelago. We used a recently published phylogeny and an extensive morphological dataset to explore whether Socotran and continental taxa differ in their dynamics of phenotypic evolution. Moreover, we used habitat data to examine if ecological specialisation is correlated with morphological change, reconstructing ancestral habitat occupancy and comparing phenotypic disparity and trait evolution between habitats. We found heterogeneity in the outcome of the colonisation of the Socotra Archipelago. Namely, only one of the three events of colonisation has resulted in an increase in body size. However, in general, Socotran species do not present higher levels or rates of morphological diversification than continental groups. Instead, habitat specialisation provides a more nuanced insight into body size and shape evolution in Pristurus. In particular, the colonisation of ground habitats appears as the main driver of morphological change, producing the highest disparity and evolutionary rates. Additionally, arboreal species show very constrained body size and head proportions, suggesting ecologically driven morphological convergence. Our results reveal a determinant role of ecological mechanisms in morphological evolution and corroborate the complexity of ecomorphological dynamics in continental-island systems.Peer reviewe

Desert lizard diversity worldwide: Effects of environment, time, and evolutionary rate

[Aim] Biodiversity is not uniformly distributed across the Earth’s surface, even among physiographically comparable biomes in different biogeographic regions. For lizards, the world’s large desert regions are characterized by extreme heterogeneity in species richness, spanning some of the most species-rich (arid Australia) and species-poor (central Asia) biomes overall. Regional differences in species diversity may arise as a consequence of the interplay of several factors (e.g., evolutionary time, diversification rate, environment), but their relative importance for biogeographic patterns remains poorly known. Here we use distributional and phylogenetic data to assess the evolutionary and ecological drivers of large-scale variation in desert lizard diversity. [Location] Deserts worldwide. [Major taxa studied] Lizards (non-snake squamates). [Methods] We specifically test whether diversity patterns are best explained by differences in the ages of arid-adapted lineages (evolutionary time hypothesis), by regional variation in speciation rate, by geographic area of the arid systems, and by spatial variation related to environment (climate, topography, and productivity). [Results] We found no effect of recent speciation rate and geographic area on differences in desert lizard diversity. We demonstrate that the extreme species richness of the Australian deserts cannot be explained by greater evolutionary time, because species began accumulating more recently there than in more species-poor arid regions. We found limited support for relationships between regional lizard richness and environmental variables, but these effects were inconsistent across deserts, showing a differential role of the environment in shaping the lizard diversity in different arid regions. [Main conclusions] Our results provide evidence against several classic hypotheses for interregional variation in species richness, but also highlight the complexity of processes underlying vertebrate community richness in the world’s great arid systems.This work has been funded by grants CGL2015-70390-P [Ministerio de Economía, Industria y Competitividad (MINECO) / European Regional Development Fund (FEDER), European Union (UE)] Spain, and PGC2018-098290-B-I00 [Ministerio de Ciencia, Innovación y Universidades (MCIU) / Agencia Estatal de Investigación (AEI) / FEDER, UE)]. H.T.-C. was funded by an FPI (Contratos predoctorales para la formación de doctores) grant (BES-2016-078341) from Agencia Estatal de Investigación (AEI), Ministerio de Economía, Industria y Competitividad (MINECO) and European Social Fund (ESF), Spai