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.

Cryptic diversity and non-adaptive radiation of montane New Guinea skinks (Papuascincus; Scincidae).

New Guinea, the world's largest and highest tropical island, has a rich but poorly known biota. Papuascincus is a genus of skinks endemic to New Guinea's mountain regions, comprising two wide-ranging species and two species known only from their type series. The phylogeny of the genus has never been examined and the relationships among its species - as well as between it and closely related taxa - are hitherto unknown. We performed the first large-scale molecular-phylogenetic study of Papuascincus, including sampling across the genus' range in Papua New Guinea. We sequenced three mitochondrial and two nuclear markers from 65 specimens of Papuascincus and reconstructed their phylogenetic relationships. We also performed species-delimitation analyses, estimated divergence times and ancestral biogeography, and examined body-size evolution within the genus. Papuascincus was strongly supported as monophyletic. It began radiating during the mid-Miocene in the area now comprising the Central Cordillera of New Guinea, then dispersed eastward colonising the Papuan Peninsula. We found evidence of extensive cryptic diversity within the genus, with between nine and 20 supported genetic lineages. These were estimated using three methods of species delimitation and predominantly occur in allopatry. Distribution and body-size divergence patterns indicated that character displacement in size took place during the evolutionary history of Papuascincus. We conclude that the genus requires comprehensive taxonomic revision and likely represents a species-rich lineage of montane skinks.

Biogeography of Mesalina (Reptilia: Lacertidae), with special emphasis on the Mesalina adramitana group from Arabia and the Socotra Archipelago.

The lacertid lizards of the genus Mesalina inhabit the arid regions of the Old World, from North Africa to NW India. Of the 19 recognized species within the genus, eleven occur in Arabia. In this study, we explore the genetic variability and phylogeographic patterns of the less studied M. adramitana group from southern Arabia and the Socotra Archipelago within the phylogenetic and biogeographic context of the entire genus. Our unprecedented sampling extends the distribution ranges of most Mesalina species and, for the first time, sequences of M. ayunensis are included in a phylogenetic analysis. We perform analyses of concatenated multilocus datasets and species trees, conduct species delimitation analyses, and estimate divergence times within a biogeographic framework. Additionally, we inferred the environmental suitability and identified dispersal corridors through which gene flow is enabled within M. adramitana. Our results show that the Socotra Archipelago was colonized approximately 7 Mya by a single oversea colonization from mainland Arabia. Then, an intra-archipelago dispersal event that occurred approximately 5 Mya resulted in the speciation between M. balfouri, endemic to Socotra, Samha and Darsa Islands, and M. kuri, endemic to Abd al Kuri Island. Similar to previous studies, we uncovered high levels of genetic diversity within the M. adramitana species-group, with two highly divergent lineages of M. adramitana living in allopatry and adapted to locally specific climatic conditions that necessitate further investigation.

An integrative study of island diversification: Insights from the endemic Haemodracon geckos of the Socotra Archipelago.

The Socotra Archipelago in the Arabian Sea is considered one of the most geo-politically isolated landforms on earth and a center of endemism. The archipelago is located at the western edge of the Indian Ocean and comprises four islands: Socotra, Darsa, Samha, and Abd al Kuri. Here we provide an integrative study on Haemodracon geckos, the sole genus of geckos strictly endemic to the archipelago. The sympatric distribution of Haemodracon riebeckii and H. trachyrhinus on Socotra Island provides a unique opportunity to explore evolutionary relationships and speciation patterns, examining the interplay between possible sympatric and allopatric scenarios. We used molecular data for phylogenetic inference, species delimitation analyses, and to infer the diversification timeframe. Multivariate statistics were used to analyze morphological data. Ecological comparisons were explored for macro-niches using species distribution models and observations were used for micro-habitat use. Haemodracon species exhibit great levels of intraspecific genetic diversity. Our calibration estimates revealed that Haemodracon diverged from its closest relative, the mainland genus Asaccus, in the Eocene, before the detachment of the archipelago. The two Haemodracon species diversified in situ on Socotra Island during the Middle Miocene, after the archipelago's isolation, into the two reciprocally monophyletic recognized species. Their divergence is associated mostly with remarkable body size differences and micro-habitat segregation, with low levels of climatic and body shape divergences within their sympatric distributions. These results display how ecological, sympatric speciation, and allopatric speciation followed by secondary contact, may both have varying roles at different evolutionary phases.

Early insularity and subsequent mountain uplift were complementary drivers of diversification in a Melanesian lizard radiation (Gekkonidae: Cyrtodactylus).

Regions with complex geological histories present a major challenge for scientists studying the processes that have shaped their biotas. The history of the vast and biologically rich tropical island of New Guinea is particularly complex and poorly resolved. Competing geological models propose New Guinea emerged as a substantial landmass either during the Mid-Miocene or as recently as the Pliocene. Likewise, the estimated timing for the uplift of the high Central Cordillera, spanning the length of the island, differs across models. Here we investigate how early islands and mountain uplift have shaped the diversification and biogeography of Cyrtodactylus geckos. Our data strongly support initial colonisation and divergence within proto-Papuan islands in the Early- to Mid-Miocene, with divergent lineages and endemic diversity concentrated on oceanic island arcs in northern New Guinea and the formerly isolated East-Papuan Composite Terrane. At least four lineages are inferred to have independently colonised hill- and lower-montane forests, indicating that mountain uplift has also played a critical role in accumulating diversity, even in this predominantly lowland lineage. Our findings suggest that substantial land in northern New Guinea and lower-montane habitats date back well into the Miocene and that insular diversification and mountain colonisation have synergistically generated diversity in the geologically complex Papuan region.

Out of Africa: Phylogeny and biogeography of the widespread genus Acanthodactylus (Reptilia: Lacertidae).

Acanthodactylus lizards are among the most diverse and widespread diurnal reptiles in the arid regions spanning from North Africa across to western India. Acanthodactylus constitutes the most species-rich genus in the family Lacertidae, with over 40 recognized species inhabiting a wide variety of dry habitats. The genus has seldom undergone taxonomic revisions, and although there are a number of described species and species-groups, their boundaries, as well as their interspecific relationships, remain largely unresolved. We constructed a multilocus phylogeny, combining data from two mitochondrial (12S, cytb) and three nuclear (MC1R, ACM4, c-mos) markers for 302 individuals belonging to 36 known species, providing the first large-scale time-calibrated molecular phylogeny of the genus. We evaluated phylogenetic relationships between and within species-groups, and assessed Acanthodactylus biogeography across its known range. Acanthodactylus cladogenesis is estimated to have originated in Africa due to vicariance and dispersal events from the Oligocene onwards. Radiation started with the separation into three clades: the Western and scutellatus clades largely distributed in North Africa, and the Eastern clade occurring mostly in south-west Asia. Most Acanthodactylus species diverged during the Miocene, possibly as a result of regional geological instability and climatic changes. We support most of the current taxonomic classifications and phylogenetic relationships, and provide genetic validity for most species. We reveal a new distinct blanfordii species-group, suggest new phylogenetic positions (A. hardyi, A. masirae), and synonymize several species and subspecies (A. lineomaculatus, A. boskianus khattensis and A. b. nigeriensis) with their phylogenetically closely-related species. We recommend a thorough systematic revision of taxa, such as A. guineensis, A. grandis, A. dumerilii, A. senegalensis and the pardalis and erythrurus species-groups, which exhibit high levels of intraspecific variability, and clear evidence of phylogenetic complexity.

Evolution around the Red Sea: Systematics and biogeography of the agamid genus Pseudotrapelus (Squamata: Agamidae) from North Africa and Arabia.

Since the Oligocene, regions adjacent to the Red Sea have experienced major environmental changes, from tectonic movements and continuous geological activity to shifting climatic conditions. The effect of these events on the distribution and diversity of the regional biota is still poorly understood. Agamid members of the genus Pseudotrapelus are diurnal, arid-adapted lizards distributed around the Red Sea from north-eastern Africa, across the mountains and rocky plateaus of the Sinai and Arabian Peninsulas northwards to Syria. Despite recent taxonomic work and the interest in the group as a model for studying biogeographic and diversity patterns of the arid areas of North Africa and Arabia, its taxonomy is poorly understood and a comprehensive phylogeny is still lacking. In this study, we analyzed 92 Pseudotrapelus specimens from across the entire distribution range of the genus. We included all known species and subspecies, and sequenced them for mitochondrial (16S, ND4 and tRNAs) and nuclear (MC1R, c-mos) markers. This enabled us to obtain the first time-calibrated molecular phylogeny of the genus, using gene trees, species trees and coalescent-based methods for species delimitation. Our results revealed Pseudotrapelus as a monophyletic genus comprised of two major clades and six independently evolving lineages. These lineages correspond to the five currently recognized species and a sixth lineage relating to the synonymized P. neumanni. The subspecific validity of P. sinaitus werneri needs further assessment as it does not form a distinct cluster relative to P. s. sinaitus. The onset of Pseudotrapelus diversification is estimated to have occurred in Arabia during the late Miocene. Radiation has likely resulted from vicariance and dispersal events due to the continued geological instability, sea level fluctuations and climatic changes within the region.

Hidden relationships and genetic diversity: Molecular phylogeny and phylogeography of the Levantine lizards of the genus Phoenicolacerta (Squamata: Lacertidae).

The Levant region witnessed dramatic tectonic events and climatic fluctuations that changed the historical landscape of the area and consequently influenced the cladogenesis and distribution of the local biota. In this study we use information from two mitochondrial and two nuclear genes and species delimitation methods in order to obtain the first robust time-calibrated molecular phylogeny of the Levantine rock lizards of the genus Phoenicolacerta. We sampled from across its distributional range with the aim to clarify its systematics, biogeography and evolution. Our results suggest that the genus includes two well-supported clades, one comprising solely the montane species Phoenicolacerta kulzeri, and the other including the three remaining species, the relatively widespread, P. laevis, the Syrian-Turkish P. cyanisparsa and the Cypriot endemic P. troodica. We found that both P. laevis and P. cyanisparsa are not monophyletic, as the Turkish populations of P. laevis branch within P. cyanisparsa. We found high levels of undescribed diversity within P. laevis which necessitate a thorough revision. We suggest that Phoenicolacerta started radiating during the mid-late Miocene, and that both vicariance and dispersal events shaped the diversification and distribution of the genus concomitantly with the formation of major geological structures and climatic fluctuations in the Levant. These results highlight the region as an important center of speciation, contributing to the species diversity of the eastern Mediterranean.

First exact record and phylogenetic position of the gecko Ptyodactylus hasselquistii (Squamata: Phyllodactylidae) from Lebanon.

The genus Ptyodactylus comprises 12 species distributed in North Africa and the Middle East. The most widely distributed species of the genus, Ptyodactylus hasselquistii, is known for its great morphological and genetic diversity, and ranges from Sudan and Egypt through Israel and Jordan towards Saudi Arabia and Yemen. In 1905 the first specimen of P. hasselquistii was collected from Lebanon, described later as a distinct subspecies, Ptyodactylus hasselquistii krameri. Here we provide a second record of P. hasselquistii from Lebanon collected in 2010, which represents the first exact record of the species in Lebanon in over 105 years. We use morphological comparisons and genetic analyses of two markers to account for the phylogenetic position of the new specimen within Ptyodactylus and to evaluate the taxonomic status of P. h. krameri. This integrative examination revealed a close association of the Lebanese specimen with nominotypic P. hasselquistii populations from Egypt and Sudan suggesting a relatively recent introduction from that general area. Similar morphological characteristics between the two Lebanese specimens and those from Egypt, and identical genetic sequences, suggest rejecting subspecific status of the Lebanese population and synonymizing the name Ptyodactylus hasselquistii krameri with the name Ptyodactylus hasselquistii.

Contributions to ophiology in Zootaxa 20012020: patterns and trends.

There are currently 3,900 recognized, extant snake species belonging to 529 genera globally (Uetz et al. 2021; this study), making snakes one of the most diverse major groups of squamates. Of the 665 currently recognized species that were described between 2001 and 2020 (a ~17% increase in total species), ~34% of these (226 species) were described in Zootaxa. This number does not include species resurrected from synonymy. The other ~66% (439) species were described in 105 other journals, bulletins or books (Fig.1a). Overall, the number of new snake species described every year is gradually increasing, and 40% of the new species described since 2011 were published in Zootaxa. Following Zootaxa, the second ranked journal, with 37 described species since 2001, is Herpetologica (Fig. 2). Anecdotally, the choice of Zootaxa as a publication outlet for new species descriptions by most authors is based on speed of publication post-acceptance, publication free of charge, relatively unconstrained number of papers published per year, relatively unconstrained manuscript length, expert section editors and reviewers, and consolidated scientometric parameters.

The demise of a wonder: Evolutionary history and conservation assessments of the Wonder Gecko Teratoscincus keyserlingii (Gekkota, Sphaerodactylidae) in Arabia.

Effective biodiversity conservation planning starts with genetic characterization within and among focal populations, in order to understand the likely impact of threats for ensuring the long-term viability of a species. The Wonder Gecko, Teratoscincus keyserlingii, is one of nine members of the genus. This species is distributed in Iran, Afghanistan, and Pakistan, with a small isolated population in the United Arab Emirates (UAE), where it is classified nationally as Critically Endangered. Within its Arabian range, anthropogenic activity is directly linked to the species' decline, with highly localised and severely fragmented populations. Here we describe the evolutionary history of Teratoscincus, by reconstructing its phylogenetic relationships and estimating its divergence times and ancestral biogeography. For conservation implications of T. keyserlingii we evaluate the genetic structure of the Arabian population using genomic data. This study supports the monophyly of most species and reveals considerable intraspecific variability in T. microlepis and T. keyserlingii, which necessitate broad systematic revisions. The UAE population of T. keyserlingii likely arrived from southern Iran during the Pleistocene and no internal structure was recovered within, implying a single population status. Regional conservation of T. keyserlingii requires improved land management and natural habitat restoration in the species' present distribution, and expansion of current protected areas, or establishment of new areas with suitable habitat for the species, mostly in northern Abu Dhabi Emirate.

To be or not to be tchernovi: a taxonomic revision of the snake genus Micrelaps (Squamata: Serpentes), in Israel.

The enigmatic snake genus Micrelaps has uncertain phylogenetic affinities. The type species of the genus, Micrelaps muelleri, inhabits the Southern Levant. Snakes inhabiting the Jordan River Valley just south of the Sea of Galilee have been described as a new species, Micrelaps tchernovi, based on their distinct colour patterns, despite M. muelleri being well known to be variable in colour-pattern traits. Here we use morphological and molecular data to examine the taxonomic status and phylogenetic affinity of Levantine Micrelaps. We show that all scalation, colour, and pattern-related traits are extremely variable across the range of these snakes. Some morphological features show clinal variation related to temperature and precipitation, and snakes with a 'tchernovi' morph are merely at one end of a continuum of morphological variation. Both 'classical muelleri' and 'tchernovi' morphs occur in syntopy in the Jordan Valley and elsewhere in Israel. Against this background of high morphological variation, neutral genetic markers show almost no differentiation between snakes, no genetic structure is evident across populations, and no differences are to be found between the two putative species. We conclude that Levantine Micrelaps belongs to a single, morphologically variable, and genetically uniform species, Micrelaps muelleri, of which M. tchernovi is a junior synonym.

Using multilocus approach to uncover cryptic diversity within Pseudotrapelus lizards from Saudi Arabia.

The agamid Pseudotrapelus lizards inhabit the mountainous areas of the Arabian Peninsula and eastern North Africa. Currently six Pseudotrapelus species are recognised, though diagnostic morphological characters are still lacking, creating great difficulty in describing new species. Recently, two specimens of Pseudotrapelus were collected from the vicinity of Riyadh in central Saudi Arabia, an area that was not sampled in previous phylogenetic studies. In here we used both mitochondrial and nuclear data to investigate the phylogenetic position of the new samples, and assess their phylogenetic relationships with the other recognised species of Pseudotrapelus from across the distribution range of the genus. We used a multilocus approach of haplotype networks, concatenated datasets and species trees, performed mitochondrial and nuclear species delimitation analyses, and estimated divergence times. In general, our results support previous molecular studies and uncover the presence of cryptic diversity within Pseudotrapelus. The phylogenetic structure of the genus is of two major clades and within them seven distinct, delimited phylogenetic groups belonging to the six recognised species and the seventh to the individuals from Riyadh. The Riyadh specimens were distinct in all analyses performed. We suggest that the new specimens from the Riyadh area are a distinct lineage, forming a clade with their phylogenetic relatives, P. sinaitus and P. chlodnickii. The clade formed by these three species diverged during the Late Miocene around 6.4 Ma, with cladogenesis possibly facilitated by vicariance and isolation caused due to climatic fluctuations and the progression of sandy areas. Our results suggest further morphological research is necessary to revise the taxonomic status of this lineage and of the entire genus.

An integrative systematic revision and biogeography of Rhynchocalamus snakes (Reptilia, Colubridae) with a description of a new species from Israel.

BACKGROUND: The colubrid snakes of the genus Rhynchocalamus are seldom studied and knowledge of their ecology and life history is scarce. Three species of Rhynchocalamus are currently recognized, R. satunini (from Turkey eastwards to Iran), R. arabicus (Yemen and Oman), and R. melanocephalus (from the Sinai Peninsula northwards to Turkey). All are slender, secretive, mainly nocturnal and rare fossorial snakes. This comprehensive study is the first to sample all known Rhynchocalamus species in order to review the intra-generic phylogenetic relationships and historical biogeography of the genus. METHODS: We revised the systematics of Rhynchocalamus using an integrative approach and evaluated its phylogeography. The phylogenetic position within the Colubridae and the phylogenetic relationships within the genus were inferred using 29 individuals belonging to the three known species, with additional sampling of two other closely-related genera, Muhtarophis and Lytorhynchus. We analysed three mitochondrial (12S, 16S, cytb) and one nuclear (c-mos) gene fragments. Phylogenetic trees were reconstructed using maximum likelihood and Bayesian inference methods; the latter method also used to provide the first time-calibrated molecular phylogeny of the genus. We generated a nuclear network and carried out a topology test and species delimitation analysis. Morphological comparisons were used to differentiate among species and to describe a new species from Israel. The studied material was comprised of 108 alcohol-preserved specimens, 15 photographs, and data from the literature for the examination of 17 mensural, 14 meristic, and two categorical characters. RESULTS: The molecular results support Rhynchocalamus as monophyletic, and as having split from its sister genus Lytorhynchus during the Late Oligocene. The three recognized species of Rhynchocalamus comprise four independently evolving groups. The molecular results reveal that the genus began to diverge during the Middle Miocene. We revealed that the best-studied species, R. melanocephalus, is paraphyletic. A population, formally ascribed to this species, from the Negev Mountain area in southern Israel is phylogenetically closer to R. arabicus from Oman than to the northern populations of the species from Israel, Syria and Turkey. Herein we describe this population as a new species: Rhynchocalamus dayanaesp. nov. DISCUSSION: We identify four species within Rhynchocalamus: R. satunini, R. arabicus, R. melanocephalus, and R. dayanaesp. nov., the latter, to the best of our knowledge, is endemic to southern Israel. The onset of Rhynchocalamus diversification is very old and estimated to have occurred during the Middle Miocene, possibly originating in the Levant region. Radiation probably resulted from vicariance and dispersal events caused by continuous geological instability, sea-level fluctuations and climatic changes within the Levant region.

Phylogeny of the genus Rhynchocalamus (Reptilia; Colubridae) with a first record from the Sultanate of Oman.

The genus Rhynchocalamus comprises three species distributed in Southwest Asia. Little is known about them, most probably because of their secretive fossorial lifestyle. The poor knowledge of the genus is even underscored by the fact that its phylogenetic affinities remained unclear until very recently. The least known of the species, Rhynchocalamus arabicus, is known only from the holotype collected in Aden, Yemen, and it has not been observed since its description in 1933. Here we provide a second record for this species, which represents the first record of this genus for Oman. This extends its range in southern Arabia by more than 1000 km. The observed specimen was determined as R. arabicus on the basis of its similarity in size, color, and scalation with the holotype. Furthermore, we sequenced three mitochondrial (12S, 16S, cytb) and one nuclear (cmos) genes for R. arabicus and for two individuals of R. melanocephalus and one R. satunini and inferred the phylogenetic relationships of all currently recognized species of the genus for the first time. The results of our phylogenetic analyses indicate that Rhynchocalamus is a member of the Western Palearctic clade of Colubrinae and is sister to Lytorhynchus, with which it forms a very well supported clade and shares some morphological characters. As our results show, R. satunini is the basal lineage of the genus and R. melanocephalus is sister to R. arabicus.