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.

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 has uncovered exceptions to this 'island effect'. Here, we tested this pattern using the geckos of the genus Pristurus from continental Arabia and Africa and the Socotra Archipelago. Using a recently published phylogeny and an extensive morphological dataset, we explore the differences in phenotypic evolution between Socotran and continental taxa. Moreover, we reconstructed ancestral habitat occupancy to examine if ecological specialization is correlated with morphological change, comparing phenotypic disparity and trait evolution between habitats. We found a heterogeneous outcome of island colonization. Namely, only one of the three colonization events resulted in a body size increase. However, in general, Socotran species do not present higher levels or rates of morphological diversification than continental groups. Instead, habitat specialization explains better the body size and shape evolution in Pristurus. Particularly, the colonization of ground habitats appears as the main driver of morphological change, producing the highest disparity and evolutionary rates. Additionally, arboreal species show very similar body size and head proportions. These results reveal a determinant role of ecological mechanisms in morphological evolution and corroborate the complexity of ecomorphological dynamics in continent-island systems.

An integrative assessment of the diversity, phylogeny, distribution, and conservation of the terrestrial reptiles (Sauropsida, Squamata) of the United Arab Emirates.

In the present study we use an unprecedented database of 5,535 distributional records to infer the diversity, ecological preferences and spatial distribution of the 60 species of terrestrial reptiles of the United Arab Emirates (UAE), and use the 57 native species to test the effectiveness of the protected areas' network in conserving this unique vertebrate fauna. We infer a time-calibrated phylogeny with 146 species of squamates and 15 genes including all UAE terrestrial reptile species to determine the phylogenetic diversity (PD) and evolutionary distinctiveness (ED) of the native species and to compare it with the distribution of the hotspots of native species richness. The results of this study indicate that the sampling effort is remarkable, covering 75% of the country's territory representing nearly the entire climatic space of the UAE defined by the mean annual temperature and the total annual precipitation, as well as the multivariate climatic space defined by a principal component analysis (PCA). Species richness is highest in the northeast of the country, in a transitional area from sandy desert to the mountainous terrain of the Hajar Mountains. The highest PD of a single square cell of 10 arc-minutes grid is of 2,430 million years (my) of accumulated evolutionary history and the strong correlation between PD and species richness suggests that the raw number of species is a good surrogate to quantify the evolutionary history (i.e., PD). The species with the highest values of ED are those in families represented by only one species in the UAE. Finally, the assessment of the UAE protected areas shows that, despite their relevance in protecting the terrestrial reptiles, they do not offer adequate protection for some threatened species. Therefore, a reassessment of some of the protected areas or the creation of species specific conservation action plans are recommended in order to ensure the preservation of the unique diversity of UAE terrestrial reptiles.

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.

Systematics of the Mesalina guttulata species complex (Squamata: Lacertidae) from Arabia with the description of two new species.

Mesalina are small diurnal lacertid lizards inhabiting arid areas from North Africa to northwestern India. Previous phylogenetic studies have shown the existence of several species complexes within the genus, some of them with high levels of undiscovered diversity. In the present study, we carry out an integrative systematic revision of the Mesalina guttulata species complex using both molecular and morphological data from across its entire distribution range in North Africa, the Middle East and Arabia. The results of the genetic analyses indicate that M. guttulata and M. bahaeldini are two allopatric sister taxa separated by the Suez Canal and that the species complex includes a further three unnamed deep phylogenetic lineages, two of them restricted to southern and southwestern Arabia and described herein as Mesalina austroarabica sp. nov. and Mesalina arnoldi sp. nov., respectively. As a result of the lack of enough material, the third deep lineage, distributed across Kuwait, Saudi Arabia and Jordan, is provisionally left undescribed. The two newly described species are characterized by their size, scale counts and tail coloration, as well as differences at the three mitochondrial and one nuclear gene analyzed in the present study.

Diversity, distribution and conservation of the terrestrial reptiles of Oman (Sauropsida, Squamata).

In the present work, we use an exceptional database including 5,359 records of 101 species of Oman's terrestrial reptiles together with spatial tools to infer the spatial patterns of species richness and endemicity, to infer the habitat preference of each species and to better define conservation priorities, with especial focus on the effectiveness of the protected areas in preserving this unique arid fauna. Our results indicate that the sampling effort is not only remarkable from a taxonomic point of view, with multiple observations for most species, but also for the spatial coverage achieved. The observations are distributed almost continuously across the two-dimensional climatic space of Oman defined by the mean annual temperature and the total annual precipitation and across the Principal Component Analysis (PCA) of the multivariate climatic space and are well represented within 17 out of the 20 climatic clusters grouping 10% of the explained climatic variance defined by PC1 and PC2. Species richness is highest in the Hajar and Dhofar Mountains, two of the most biodiverse areas of the Arabian Peninsula, and endemic species richness is greatest in the Jebel Akhdar, the highest part of the Hajar Mountains. Oman's 22 protected areas cover only 3.91% of the country, including within their limits 63.37% of terrestrial reptiles and 50% of all endemics. Our analyses show that large areas of the climatic space of Oman lie outside protected areas and that seven of the 20 climatic clusters are not protected at all. The results of the gap analysis indicate that most of the species are below the conservation target of 17% or even the less restrictive 12% of their total area within a protected area in order to be considered adequately protected. Therefore, an evaluation of the coverage of the current network of protected areas and the identification of priority protected areas for reptiles using reserve design algorithms are urgently needed. Our study also shows that more than half of the species are still pending of a definitive evaluation by the International Union for Conservation of Nature (IUCN).

Cryptic diversity in Ptyodactylus (Reptilia: Gekkonidae) from the northern Hajar Mountains of Oman and the United Arab Emirates uncovered by an integrative taxonomic approach.

The Hajar Mountains of south-eastern Arabia form an isolated massif surrounded by the sea to the east and by a large desert to the west. As a result of their old geological origin, geographical isolation, complex topography and local climate, these mountains provide an important refuge for endemic and relict species of plants and animals. With 19 species restricted to the Hajar Mountains, reptiles are the vertebrate group with the highest level of endemicity, becoming an excellent model for understanding the patterns and processes that generate and shape diversity in this arid mountain range. The geckos of the Ptyodactylus hasselquistii species complex are the largest geckos in Arabia and are found widely distributed across the Arabian Mountains, constituting a very important component of the reptile mountain fauna. Preliminary analyses suggested that their diversity in the Hajar Mountains may be higher than expected and that their systematics should be revised. In order to tackle these questions, we inferred a nearly complete calibrated phylogeny of the genus Ptyodactylus to identify the origin of the Hajar Mountains lineages using information from two mitochondrial and four nuclear genes. Genetic variability within the Hajar Mountains was further investigated using 68 specimens of Ptyodactylus from 46 localities distributed across the entire mountain range and sequenced for the same genes as above. The molecular phylogenies and morphological analyses as well as niche comparisons indicate the presence of two very old sister cryptic species living in allopatry: one restricted to the extreme northern Hajar Mountains and described as a new species herein; the other distributed across the rest of the Hajar Mountains that can be confidently assigned to the species P. orlovi. Similar to recent findings in the geckos of the genus Asaccus, the results of the present study uncover more hidden diversity in the northern Hajar Mountains and stress once again the importance of this unique mountain range as a hot spot of biodiversity and a priority focal point for reptile conservation in Arabia.

The complete mitochondrial genome of Pristurus rupestris rupestris.

Pristurus rupestris rupestris is a gecko of the family Sphaerodactylidae adapted to the arid habitat found in the Hajar Mountains of southeastern Arabia. The complete mitochondrial genome was obtained with Illumina sequencing. The sequenced mitogenome has 13 protein-coding genes, 22 tRNAs, two rRNA genes and two non-coding regions, totalling 16,993 bp. The AT content of the obtained sequence is 52.1% (A:28.7%, T:23.4%, G:14.7%, C:33.2%). The control region has an AT content of 54.3% and a length of 1558 bp.

Microendemicity in the northern Hajar Mountains of Oman and the United Arab Emirates with the description of two new species of geckos of the genus Asaccus (Squamata: Phyllodactylidae).

BACKGROUND: The Hajar Mountains of Oman and the United Arab Emirates (UAE) is the highest mountain range in Eastern Arabia. As a result of their old geological origin, geographical isolation, complex topography and local climate, these mountains provide an important refuge for endemic and relict species of plants and animals with strong Indo-Iranian affinities. Among vertebrates, the rock climbing nocturnal geckos of the genus Asaccus represent the genus with the highest number of endemic species in the Hajar Mountains. Recent taxonomic studies on the Zagros populations of Asaccus have shown that this genus is much richer than it was previously thought and preliminary morphological and molecular data suggest that its diversity in Arabia may also be underestimated. METHODS: A total of 83 specimens originally classified as Asaccus caudivolvulus (including specimens of the two new species described herein), six other Asaccus species from the Hajar and the Zagros Mountains and two representatives of the genus Haemodracon were sequenced for up to 2,311 base pairs including the mitochondrial 12S and cytb and the nuclear c-mos, MC1R and ACM4 genes. Phylogenetic relationships were inferred using both Bayesian and maximum-likelihood approaches and the former method was also used to calibrate the phylogenetic tree. Haplotype networks and phylogenetic trees were inferred from the phased nuclear genes only. Sixty-one alcohol-preserved adult specimens originally classified as Asaccus caudivolvulus from the northern Hajar Mountains were examined for 13 morphometric and the five meristic variables using multivariate methods and were also used to diagnose and describe the two new species. RESULTS: The results of the molecular and morphological analyses indicate that the species originally classified as Asaccus caudivolvulus is, in fact, an assemblage of three different species that started diversifying during the Mid-Miocene. The molecular phylogenies consistently recovered the Hajar endemic A. montanus as sister taxon to all the other Asaccus species included in the analyses, rendering the Arabian species of Asaccus polyphyletic. DISCUSSION: Using this integrative approach we have uncovered a very old diversification event that has resulted in a case of microendemicity, where three morphologically and ecologically similar medium-sized lizard species coexist in a very short and narrow mountain stretch. Asaccus caudivolvulus is restricted to a small coastal area of the UAE and at risk from heavy development, while the two new species described herein are widely distributed across the northern tip of the Hajar Mountains and seem to segregate in altitude when found in close proximity in the Musandam Peninsula (Oman). Similarly to other integrative analyses of Hajar reptiles, this study highlights the high level of diversity and endemicity of this arid mountain range, underscoring its status as one of the top hotspots of reptile diversity in Arabia.

Unexpectedly High Levels of Cryptic Diversity Uncovered by a Complete DNA Barcoding of Reptiles of the Socotra Archipelago.

Few DNA barcoding studies of squamate reptiles have been conducted. Due to the significance of the Socotra Archipelago (a UNESCO Natural World Heritage site and a biodiversity hotspot) and the conservation interest of its reptile fauna (94% endemics), we performed the most comprehensive DNA barcoding study on an island group to date to test its applicability to specimen identification and species discovery. Reptiles constitute Socotra's most important vertebrate fauna, yet their taxonomy remains under-studied. We successfully DNA-barcoded 380 individuals of all 31 presently recognized species. The specimen identification success rate is moderate to high, and almost all species presented local barcoding gaps. The unexpected high levels of intra-specific variability found within some species suggest cryptic diversity. Species richness may be under-estimated by 13.8-54.4%. This has implications in the species' ranges and conservation status that should be considered for conservation planning. Other phylogenetic studies using mitochondrial and nuclear markers are congruent with our results. We conclude that, despite its reduced length (663 base pairs), cytochrome c oxidase 1, COI, is very useful for specimen identification and for detecting intra-specific diversity, and has a good phylogenetic signal. We recommend DNA barcoding to be applied to other biodiversity hotspots for quickly and cost-efficiently flagging species discovery, preferentially incorporated into an integrative taxonomic framework.

Phylogenetic relationships of Semaphore geckos (Squamata: Sphaerodactylidae: Pristurus) with an assessment of the taxonomy of Pristurus rupestris.

A molecular phylogeny of the sphaerodactylid geckos of the genus Pristurus is inferred based on an alignment of 1845 base pairs (bp) of concatenated mitochondrial (12S) and nuclear (acm4, cmos, rag1 and rag2) genes for 80 individuals, representing 18 of the 23-26 species, and the three subspecies of P. rupestris. The results indicate that P. rupestris is polyphyletic and includes two highly divergent clades: the eastern clade, found in coastal Iran and throughout the Hajar Mountain range in northern Oman and eastern UAE; and the western clade, distributed from central coastal Oman, through Yemen, Saudi Arabia and north to southern Jordan. Inferred haplotype networks for the four nuclear genes show that the eastern and western clades of "P. rupestris" are highly differentiated and do not share any alleles. Moreover, although the two clades are differentiated by a morphological multivariate analysis, no one character or set of characters was found to be diagnostic. Based on the molecular analysis of specimens from the type locality of P. rupestris rupestris, the name P. rupestris is applied to the eastern clade. The name that should apply to the western clade cannot be clarified until morphological and genetic data for "P. rupestris" is available from the vicinity of Bosaso, Somalia, and therefore we refer to it as Pristurus sp. 1. The phylogenetic tree of Pristurus supports the hypothesis that P. celerrimus is sister to all the other species in the analyses and that the Socotra Archipelago was independently colonized a minimum of two times.