North African fox genomes show signatures of repeated introgression and adaptation to life in deserts.

Elucidating the evolutionary process of animal adaptation to deserts is key to understanding adaptive responses to climate change. Here we generated 82 individual whole genomes of four fox species (genus Vulpes) inhabiting the Sahara Desert at different evolutionary times. We show that adaptation of new colonizing species to a hot arid environment has probably been facilitated by introgression and trans-species polymorphisms shared with older desert resident species, including a putatively adaptive 25 Mb genomic region. Scans for signatures of selection implicated genes affecting temperature perception, non-renal water loss and heat production in the recent adaptation of North African red foxes (Vulpes vulpes), after divergence from Eurasian populations approximately 78 thousand years ago. In the extreme desert specialists, Rueppell's fox (V. rueppellii) and fennec (V. zerda), we identified repeated signatures of selection in genes affecting renal water homeostasis supported by gene expression and physiological differences. Our study provides insights into the mechanisms and genetic underpinnings of a natural experiment of repeated adaptation to extreme conditions.

First complete mitochondrial genome of the Saharan striped polecat (Ictonyx libycus).

The Saharan striped polecat (Ictonyx libycus) is endemic to Africa, inhabiting the edges of the Saharan Desert. Little is known about the biology or genetic status of this member of the weasel family (Mustelidae). We present the first complete mitochondrial genome of the Saharan striped polecat, assembled from data generated using a genome skimming approach. The assembled mitogenome is 16,549 bps in length and consists of 37 genes including 13 protein-coding genes, 2 rRNAs, 22 tRNAs, an origin of replication, and a control region. Phylogenetic analysis confirmed the placement of the Saharan striped polecat within the subfamily Ictonychinae.

Life in Deserts: The Genetic Basis of Mammalian Desert Adaptation.

Deserts are among the harshest environments on Earth. The multiple ages of different deserts and their global distribution provide a unique opportunity to study repeated adaptation at different timescales. Here, we summarize recent genomic research on the genetic mechanisms underlying desert adaptations in mammals. Several studies on different desert mammals show large overlap in functional classes of genes and pathways, consistent with the complexity and variety of phenotypes associated with desert adaptation to water and food scarcity and extreme temperatures. However, studies of desert adaptation are also challenged by a lack of accurate genotype-phenotype-environment maps. We encourage development of systems that facilitate functional analyses, but also acknowledge the need for more studies on a wider variety of desert mammals.

Systematics, biogeography and evolution of the Saharo-Arabian naked-toed geckos genus Tropiocolotes.

Plate tectonics constitute one of the main mechanisms of biological diversification on Earth, often being associated with cladogenetic events at different phylogenetic levels, as well as with exchange of faunas and floras across previously isolated biogeographic regions. North Africa and Arabia share a complex geological history that dates back to the break-up of the Arabian plate from the African plate ~30-25 Mya, followed by various geological events, such as the formation of the Red Sea or the connection between the African, Arabian and Eurasian plates. Species with Saharo-Arabian distributions have shown a close association between their evolutionary history and these geological events. In this study, we investigate the systematics, biogeography and evolution of the genus Tropiocolotes, a group of small ground-dwelling geckos, comprised by 12 species distributed from the Atlantic coast of North Africa to southwestern Iran. Species delimitation analyses uncovered the existence of high levels of undescribed diversity, with forms here considered at the species level including Tropiocolotes tripolitanus (Mauritania and southern Morocco), T. nattereri (southern Israel) and T. scorteccii (Yemen and Oman). Phylogenetic and biogeographic analyses recovered two main clades, an exclusively African clade and a Saharo-Arabian clade, that split ~25 Mya following the vicariant event mediated by the separation of the Arabian and African plates. The complex geological activity around the Red Sea is associated with the diversification within the Saharo-Arabian clade, including the colonization of North Africa from a second Tropiocolotes group. Results also provide new insights into the geographic distribution of Tropiocolotes nubicus, previously considered as exclusively associated to the Nile River valley, extending its known distribution further west, up to the Central Mountains of the Sahara. Accordingly, the Nile River seems to act as a major biogeographic barrier, separating Tropiocolotes nubicus and T. steudneri in their western and eastern margins, respectively.

The evolutionary history of the Cape hare (Lepus capensis sensu lato): insights for systematics and biogeography.

Inferring the phylogeography of species with large distributions helps deciphering major diversification patterns that may occur in parallel across taxa. Here, we infer the evolutionary history of the Cape hare, Lepus capensis sensu lato, a species distributed from southern Africa to Asia, by analyzing variation at 18 microsatellites and 9 DNA (1 mitochondrial and 8 nuclear) sequenced loci, from field and museum-collected samples. Using a combination of assignment and coalescent-based methods, we show that the Cape hare is composed of five evolutionary lineages, distributed in distinct biogeographic regions-north-western Africa, eastern Africa, southern Africa, the Near East and the Arabian Peninsula. A deep phylogenetic break possibly dating to the Early Pleistocene was inferred between the African and Asian L. capensis groups, and the latter appear more closely related to other Eurasian hare species than to African Cape hares. The inferred phylogeographic structure is shared by numerous taxa distributed across the studied range, suggesting that environmental changes, such as the progressive aridification of the Saharo-Arabian desert and the fluctuations of savannah habitats in Sub-Saharan Africa, had comparable impacts across species. Fine-scale analyses of the western Sahara-Sahel populations showed rich fragmentation patterns for mitochondrial DNA but not for microsatellites, compatible with the environmental heterogeneity of the region and female philopatry. The complex evolutionary history of L. capensis sensu lato, which possibly includes interspecific gene flow, is not reflected by taxonomy. Integrating evolutionary inference contributes to an improved characterization of biodiversity, which is fundamental to foster the conservation of relevant evolutionary units.

Challenges for assessing vertebrate diversity in turbid Saharan water-bodies using environmental DNA.

The Sahara desert is the largest warm desert in the world and a poorly explored area. Small water-bodies occur across the desert and are crucial habitats for vertebrate biodiversity. Environmental DNA (eDNA) is a powerful tool for species detection and is being increasingly used to conduct biodiversity assessments. However, there are a number of difficulties with sampling eDNA from such turbid water-bodies and it is often not feasible to rely on electrical tools in remote desert environments. We trialled a manually powered filtering method in Mauritania, using pre-filtration to circumvent problems posed by turbid water in remote arid areas. From nine vertebrate species expected in the water-bodies, four were detected visually, two via metabarcoding, and one via both methods. Difficulties filtering turbid water led to severe constraints, limiting the sampling protocol to only one sampling point per study site, which alone may largely explain why many of the expected vertebrate species were not detected. The amplification of human DNA using general vertebrate primers is also likely to have contributed to the low number of taxa identified. Here we highlight a number of challenges that need to be overcome to successfully conduct metabarcoding eDNA studies for vertebrates in desert environments in Africa.

Repeated evolution of camouflage in speciose desert rodents.

There are two main factors explaining variation among species and the evolution of characters along phylogeny: adaptive change, including phenotypic and genetic responses to selective pressures, and phylogenetic inertia, or the resemblance between species due to shared phylogenetic history. Phenotype-habitat colour match, a classic Darwinian example of the evolution of camouflage (crypsis), offers the opportunity to test the importance of historical versus ecological mechanisms in shaping phenotypes among phylogenetically closely related taxa. To assess it, we investigated fur (phenotypic data) and habitat (remote sensing data) colourations, along with phylogenetic information, in the species-rich Gerbillus genus. Overall, we found a strong phenotype-habitat match, once the phylogenetic signal is taken into account. We found that camouflage has been acquired and lost repeatedly in the course of the evolutionary history of Gerbillus. Our results suggest that fur colouration and its covariation with habitat is a relatively labile character in mammals, potentially responding quickly to selection. Relatively unconstrained and substantial genetic basis, as well as structural and functional independence from other fitness traits of mammalian colouration might be responsible for that observation.

An Ecoregion-Based Approach to Protecting Half the Terrestrial Realm.

We assess progress toward the protection of 50% of the terrestrial biosphere to address the species-extinction crisis and conserve a global ecological heritage for future generations. Using a map of Earth's 846 terrestrial ecoregions, we show that 98 ecoregions (12%) exceed Half Protected; 313 ecoregions (37%) fall short of Half Protected but have sufficient unaltered habitat remaining to reach the target; and 207 ecoregions (24%) are in peril, where an average of only 4% of natural habitat remains. We propose a Global Deal for Nature-a companion to the Paris Climate Deal-to promote increased habitat protection and restoration, national- and ecoregion-scale conservation strategies, and the empowerment of indigenous peoples to protect their sovereign lands. The goal of such an accord would be to protect half the terrestrial realm by 2050 to halt the extinction crisis while sustaining human livelihoods.

Genome-wide Evidence Reveals that African and Eurasian Golden Jackals Are Distinct Species.

The golden jackal of Africa (Canis aureus) has long been considered a conspecific of jackals distributed throughout Eurasia, with the nearest source populations in the Middle East. However, two recent reports found that mitochondrial haplotypes of some African golden jackals aligned more closely to gray wolves (Canis lupus), which is surprising given the absence of gray wolves in Africa and the phenotypic divergence between the two species. Moreover, these results imply the existence of a previously unrecognized phylogenetically distinct species despite a long history of taxonomic work on African canids. To test the distinct-species hypothesis and understand the evolutionary history that would account for this puzzling result, we analyzed extensive genomic data including mitochondrial genome sequences, sequences from 20 autosomal loci (17 introns and 3 exon segments), microsatellite loci, X- and Y-linked zinc-finger protein gene (ZFX and ZFY) sequences, and whole-genome nuclear sequences in African and Eurasian golden jackals and gray wolves. Our results provide consistent and robust evidence that populations of golden jackals from Africa and Eurasia represent distinct monophyletic lineages separated for more than one million years, sufficient to merit formal recognition as different species: C. anthus (African golden wolf) and C. aureus (Eurasian golden jackal). Using morphologic data, we demonstrate a striking morphologic similarity between East African and Eurasian golden jackals, suggesting parallelism, which may have misled taxonomists and likely reflects uniquely intense interspecific competition in the East African carnivore guild. Our study shows how ecology can confound taxonomy if interspecific competition constrains size diversification.

Species on the rocks: Systematics and biogeography of the rock-dwelling Ptyodactylus geckos (Squamata: Phyllodactylidae) in North Africa and Arabia.

The understanding of the diversity of species in the Palearctic and the processes that have generated it is still weak for large parts of the arid areas of North Africa and Arabia. Reptiles are among their most remarkable representatives, with numerous groups well adapted to the diverse environments. The Ptyodactylus geckos are a strictly rock-dwelling genus with homogeneous morphology distributed across mountain formations and rocky plateaus from the western African ranges in Mauritania and the Maghreb to the eastern tip of the Arabian Peninsula, with an isolated species in southern Pakistan. Here, we use a broad sampling of 378 specimens, two mitochondrial (12S and cytb) and four nuclear (c-mos, MC1R, ACM4, RAG2) markers in order to obtain the first time-calibrated molecular phylogeny of the genus and place its diversification in a temporal framework. The results reveal high levels of intraspecific variability, indicative of undescribed diversity, and they do not support the monophyly of one species (P. ragazzii). Ptyodactylus species are allopatric across most of their range, which may relate to their high preference for the same type of structural habitat. The onset of their diversification is estimated to have occurred in the Late Oligocene, while that of several deep clades in the phylogeny took place during the Late Miocene, a period when an increase in aridification in North Africa and Arabia initiated.

Molecular assessment of Hepatozoon (Apicomplexa: Adeleorina) infections in wild canids and rodents from north Africa, with implications for transmission dynamics across taxonomic groups.

Parasites play a major role in ecosystems, and understanding of host-parasite interactions is important for predicting parasite transmission dynamics and epidemiology. However, there is still a lack of knowledge about the distribution, diversity, and impact of parasites in wildlife, especially from remote areas. Hepatozoon is a genus of apicomplexan parasites that is transmitted by ingestion of infected arthropod vectors. However, alternative modes of transmission have been identified such as trophic transmission. Using the 18S rRNA gene as a marker, we provide an assessment of Hepatozoon prevalence in six wild canid and two rodent species collected between 2003 and 2012 from remote areas in North Africa. By combining this with other predator-prey systems in a phylogenetic framework, we investigate Hepatozoon transmission dynamics in distinct host taxa. Prevalence was high overall among host species (African jerboa Jaculus jaculus [17/47, 36%], greater Egyptian jerboa Jaculus orientalis [5/7, 71%], side-striped jackal Canis adustus [1/2, 50%], golden jackal Canis aureus [6/32, 18%], pale fox Vulpes pallida [14/28, 50%], Rüppell's fox Vulpes rueppellii [6/11, 55%], red fox Vulpes vulpes [8/16, 50%], and fennec fox Vulpes zerda [7/11, 42%]). Phylogenetic analysis showed further evidence of occasional transmission of Hepatozoon lineages from prey to canid predators, which seems to occur less frequently than in other predator-prey systems such as between snakes and lizards. Due to the complex nature of the Hepatozoon lifecycle (heteroxenous and vector-borne), future studies on these wild host species need to clarify the dynamics of alternative modes of Hepatozoon transmission and identify reservoir and definitive hosts in natural populations. We also detected putative Babesia spp. (Apicomplexa: Piroplasmida) infections in two canid species from this region, V. pallida (1/28) and V. zerda (1/11).

Patterns of genetic diversity in Hepatozoon spp. infecting snakes from North Africa and the Mediterranean Basin.

Species of Hepatozoon Miller, 1908 are blood parasites most commonly found in snakes but some have been described from all tetrapod groups and a wide variety of hematophagous invertebrates. Previous studies have suggested possible associations between Hepatozoon spp. found in predators and prey. Particularly, some saurophagous snakes from North Africa and the Mediterranean region have been found to be infected with Hepatozoon spp. similar to those of various sympatric lizard hosts. In this study, we have screened tissue samples of 111 North African and Mediterranean snakes, using specific primers for the 18S rRNA gene. In the phylogenetic analysis, the newly-generated Hepatozoon spp. sequences grouped separately into five main clusters. Three of these clusters were composed by Hepatozoon spp. also found in snakes and other reptiles from the Mediterranean Basin and North Africa. In the other two clusters, the new sequences were not closely related to geographically proximate known sequences. The phylogeny of Hepatozoon spp. inferred here was not associated with intermediate host taxonomy or geographical distribution. From the other factors that could explain these evolutionary patterns, the most likely seems series of intermediate hosts providing similar ribotypes of Hepatozoon and a high prevalence of host shifts for Hepatozoon spp. This is indicated by ribotypes of high similarity found in different reptile families, as well as by divergent ribotypes found in the same host species. This potentially low host specificity has profound implications for the systematics of Hepatozoon spp.

Hybridization at an ecotone: ecological and genetic barriers between three Iberian vipers.

The formation of stable genetic boundaries between emerging species is often diagnosed by reduced hybrid fitness relative to parental taxa. This reduced fitness can arise from endogenous and/or exogenous barriers to gene flow. Although detecting exogenous barriers in nature is difficult, we can estimate the role of ecological divergence in driving species boundaries by integrating molecular and ecological niche modelling tools. Here, we focus on a three-way secondary contact zone between three viper species (Vipera aspis, V. latastei and V. seoanei) to test for the contribution of ecological divergence to the development of reproductive barriers at several species traits (morphology, nuclear DNA and mitochondrial DNA). Both the nuclear and mitochondrial data show that all taxa are genetically distinct and that the sister species V. aspis and V. latastei hybridize frequently and backcross over several generations. We find that the three taxa have diverged ecologically and meet at a hybrid zone coincident with a steep ecotone between the Atlantic and Mediterranean biogeographical provinces. Integrating landscape and genetic approaches, we show that hybridization is spatially restricted to habitats that are suboptimal for parental taxa. Together, these results suggest that niche separation and adaptation to an ecological gradient confer an important barrier to gene flow among taxa that have not achieved complete reproductive isolation.

Unravelling biodiversity, evolution and threats to conservation in the Sahara-Sahel.

Deserts and arid regions are generally perceived as bare and rather homogeneous areas of low diversity. The Sahara is the largest warm desert in the world and together with the arid Sahel displays high topographical and climatic heterogeneity, and has experienced recent and strong climatic oscillations that have greatly shifted biodiversity distribution and community composition. The large size, remoteness and long-term political instability of the Sahara-Sahel, have limited knowledge on its biodiversity. However, over the last decade, there have been an increasing number of published scientific studies based on modern geomatic and molecular tools, and broad sampling of taxa of these regions. This review tracks trends in knowledge about biodiversity patterns, processes and threats across the Sahara-Sahel, and anticipates needs for biodiversity research and conservation. Recent studies are changing completely the perception of regional biodiversity patterns. Instead of relatively low species diversity with distribution covering most of the region, studies now suggest a high rate of endemism and larger number of species, with much narrower and fragmented ranges, frequently limited to micro-hotspots of biodiversity. Molecular-based studies are also unravelling cryptic diversity associated with mountains, which together with recent distribution atlases, allows identifying integrative biogeographic patterns in biodiversity distribution. Mapping of multivariate environmental variation (at 1 km × 1 km resolution) of the region illustrates main biogeographical features of the Sahara-Sahel and supports recently hypothesised dispersal corridors and refugia. Micro-scale water-features present mostly in mountains have been associated with local biodiversity hotspots. However, the distribution of available data on vertebrates highlights current knowledge gaps that still apply to a large proportion of the Sahara-Sahel. Current research is providing insights into key evolutionary and ecological processes, including causes and timing of radiation and divergence for multiple taxa, and associating the onset of the Sahara with diversification processes for low-mobility vertebrates. Examples of phylogeographic patterns are showing the importance of allopatric speciation in the Sahara-Sahel, and this review presents a synthetic overview of the most commonly hypothesised diversification mechanisms. Studies are also stressing that biodiversity is threatened by increasing human activities in the region, including overhunting and natural resources prospection, and in the future by predicted global warming. A representation of areas of conflict, landmines, and natural resources extraction illustrates how human activities and regional insecurity are hampering biodiversity research and conservation. Although there are still numerous knowledge gaps for the optimised conservation of biodiversity in the region, a set of research priorities is provided to identify the framework data needed to support regional conservation planning.

Climate change is predicted to negatively influence Moroccan endemic reptile richness. Implications for conservation in protected areas.

The identification of species-rich areas and their prognosticated turnover under climate change are crucial for the conservation of endemic taxa. This study aims to identify areas of reptile endemicity richness in a global biodiversity hot spot (Morocco) under current and future climatic conditions and to investigate the role of protected areas in biodiversity conservation under climate change. Species distribution models (SDM) were performed over the distribution of 21 endemic reptiles, combined to estimate current species richness at 1 × 1 km resolution and projected to years 2050 and 2080 according to distinct story lines and ensemble global circulation models, assuming unlimited and null dispersion ability. Generalized additive models were performed between species richness and geographic characteristics of 43 protected areas. SDM found precipitation as the most important factor related to current species distributions. Important reductions in future suitable areas were predicted for 50 % of species, and four species were identified as highly vulnerable to extinction. Drastic reductions in species-rich areas were predicted for the future, with considerable variability between years and dispersal scenarios. High turnover rates of species composition were predicted for eastern Morocco, whereas low values were forecasted for the Northern Atlantic coast and mountains. Species richness for current and future conditions was significantly related to the altitude and latitude of protected areas. Protected areas located in mountains and/or in the Northern Atlantic coast were identified as refugia, where population monitoring and conservation management is needed.

Phylogeny of North African Agama lizards (Reptilia: Agamidae) and the role of the Sahara desert in vertebrate speciation.

The origin of Saharan biodiversity is poorly understood, in part because the geological and paleoclimatic events that presumably shaped species diversity are still controversial, but also because few studies have explored causal explanations for the origin of Saharan diversity using a phylogenetic framework. Here, we use mtDNA (16S and ND4 genes) and nDNA (MC1R and CMOS genes) to infer the relationships and biogeographic history of North African agamas (genus Agama). Agamas are conspicuous, diverse and abundant African lizards that also occur in the Saharan xeric and mesic environments. Our results revealed the presence of three Agama lineages in North Africa: one Afrotropical, one Sahelo-Saharan, and one broadly distributed in North Africa and mainly Saharan. Southern Mauritania contains the highest known diversity, with all three lineages present. Results suggest that agamas colonized the Sahara twice, but only one lineage was able to radiate and diversify there. Species in the Saharan lineage are mostly allopatric, and their splitting, genetic diversity and distribution are greatly explained by mountain ranges. One species in this lineage has colonized the Mediterranean climatic zone (A. impalearis), and another one the Sahel savannah (A. boueti). The other lineage to colonize the Sahara corresponds to A. boulengeri, an eminently Sahelian species that also inhabits Saharan mountain ranges in Mauritania and Mali. Phylogenetic analyses indicate that allopatric montane populations within some currently recognized species are also genetically divergent. Our study therefore concludes that vicariant speciation is a leading motor of species diversification in the area: Inside the Sahara, associated to mountain-ranges isolated by dune seas and bare plains; outside, associated to less harsh climates to the North and South. Paleoclimatic oscillations are suggested as causal explanations of the vicariant distribution and origin of species. Agamas are thought to have colonized northern Africa during wet periods, with subsequent dry periods fragmenting species distribution and leading to allopatric populations associated to milder and wetter climates in the Mediterranean, Sahel, and in Saharan mountains, in an island-model fashion. Finally, our results support the synonymization of A. castroviejoi with A. boueti, the reciprocal monophyly of all other North African agamas, and suggest one candidate species within A. boulengeri.

Postglacial colonization of Europe by the barbastelle bat: agreement between molecular data and past predictive modelling.

The barbastelle (Barbastella barbastellus) is a rare forest bat with a wide distribution in Europe. Here, we combine results from the analysis of two mtDNA fragments with species distribution modelling to determine glacial refugia and postglacial colonization routes. We also investigated whether niche conservatism occurs in this species. Glacial refugia were identified in the three southern European peninsulas: Iberia, Italy and the Balkans. These latter two refugia played a major role in the postglacial colonization process, with their populations expanding to England and central Europe, respectively. Palaeo-distribution models predicted that suitable climatic conditions existed in the inferred refugia during the last glacial maximum (LGM). Nevertheless, the overlap between the current and the LGM distributions was almost inexistent in Italy and in the Balkans, meaning that B. barbastellus populations were forced to shift range between glacial and interglacial periods, a process that probably caused some local extinctions. In contrast, Iberian populations showed a 'refugia within refugium' pattern, with two unconnected areas containing stable populations (populations that subsisted during both glacial and interglacial phases). Moreover, the match between LGM models and the refugial areas determined by molecular analysis supported the hypothesis of niche conservatism in B. barbastellus. We argue that geographic patterns of genetic structuring, altogether with the modelling results, indicate the existence of four management units for conservation: Morocco, Iberia, Italy and UK, and Balkans and central Europe. In addition, all countries sampled possessed unique gene pools, thus stressing the need for the conservation of local populations.

Crocodiles in the Sahara desert: an update of distribution, habitats and population status for conservation planning in Mauritania.

BACKGROUND: Relict populations of Crocodylus niloticus persist in Chad, Egypt and Mauritania. Although crocodiles were widespread throughout the Sahara until the early 20(th) century, increased aridity combined with human persecution led to local extinction. Knowledge on distribution, occupied habitats, population size and prey availability is scarce in most populations. This study evaluates the status of Saharan crocodiles and provides new data for Mauritania to assist conservation planning. METHODOLOGY/PRINCIPAL FINDINGS: A series of surveys in Mauritania detected crocodile presence in 78 localities dispersed across 10 river basins and most tended to be isolated within river basins. Permanent gueltas and seasonal tâmoûrts were the most common occupied habitats. Crocodile encounters ranged from one to more than 20 individuals, but in most localities less than five crocodiles were observed. Larger numbers were observed after the rainy season and during night sampling. Crocodiles were found dead in between water points along dry river-beds suggesting the occurrence of dispersal. CONCLUSION/SIGNIFICANCE: Research priorities in Chad and Egypt should focus on quantifying population size and pressures exerted on habitats. The present study increased in by 35% the number of known crocodile localities in Mauritania. Gueltas are crucial for the persistence of mountain populations. Oscillations in water availability throughout the year and the small dimensions of gueltas affect biological traits, including activity and body size. Studies are needed to understand adaptation traits of desert populations. Molecular analyses are needed to quantify genetic variability, population sub-structuring and effective population size, and detect the occurrence of gene flow. Monitoring is needed to detect demographical and genetical trends in completely isolated populations. Crocodiles are apparently vulnerable during dispersal events. Awareness campaigns focusing on the vulnerability and relict value of crocodiles should be implemented. Classification of Mauritanian mountains as protected areas should be prioritised.