Genetic depletion does not prevent rapid evolution in island-introduced lizards.

Experimental introductions of species have provided some of the most tractable examples of rapid phenotypic changes, which may reflect plasticity, the impact of stochastic processes, or the action of natural selection. Yet to date, very few studies have investigated the neutral and potentially adaptive genetic impacts of experimental introductions. We dissect the role of these processes in shaping the population differentiation of wall lizards in three Croatian islands (Susac, Pod Kopiste, and Pod Mrcaru), including the islet of Pod Mrcaru, where experimentally introduced lizards underwent rapid (~30 generations) phenotypic changes associated with a shift from an insectivorous to a plant-based diet. Using a genomic approach (~82,000 ddRAD loci), we confirmed a founder effect during introduction and very low neutral genetic differentiation between the introduced population and its source. However, genetic depletion did not prevent rapid population growth, as the introduced lizards exhibited population genetic signals of expansion and are known to have reached a high density. Our genome-scan analysis identified just a handful of loci showing large allelic shifts between ecologically divergent populations. This low overall signal of selection suggests that the extreme phenotypic differences observed among populations are determined by a small number of large-effect loci and/or that phenotypic plasticity plays a major role in phenotypic changes. Nonetheless, functional annotation of the outlier loci revealed some candidate genes relevant to diet-induced adaptation, in agreement with the hypothesis of directional selection. Our study provides important insights on the evolutionary potential of bottlenecked populations in response to new selective pressures on short ecological timescales.

Erratum: Corrigendum: Salvi D, Al-Kandari M, Oliver PG, Berrilli E, Garzia M (2022) Cryptic marine diversity in the northern Arabian Gulf: an integrative approach uncovers a new species of oyster (Bivalvia: Ostreidae), Ostreaoleomargarita. Journal of Zoological Systematics and Evolutionary Research 2022: 7058975. https://doi.org/10.1155/2022/7058975.

[This corrects the article DOI: 10.1155/2022/7058975.].

Climbing on the La Canna Volcanic Sea Stack to Obtain First-Hand Data on the Tiniest Population of the Critically Endangered Aeolian Wall Lizard Podarcis raffonei.

Among the extant populations of the critically endangered Aeolian wall lizard, the most vulnerable is the one surviving on La Canna, a columnar volcanic stack off the Filicudi Island. Here, I report the results of the first climbing expedition by a biologist on La Canna, that contributed direct observations and updated information on the size, morphology, and genetic variability of this population. Lizard density at the sampling site (a small terrace at 50 m of elevation) was 1.7 m-2, twice of a previous estimate. Standard methods for estimating population size are unsuitable for La Canna. An educated guess of about a hundred individuals can be drawn, considering the extent of habitat available on the stack and the number of observed lizards. Lizards on La Canna were not fearless, despite what was reported by alpinists, possibly because of aggressive intraspecific interactions or high environmental temperatures during sampling. Biometric data significantly extend the body size of La Canna's lizards and indicate that it is not smaller than other P. raffonei populations. A complete lack of genetic diversity was found at the mitochondrial nd4 gene, in line with previous allozyme data and with estimates on other microinsular Podarcis populations. The small size of the La Canna population implies severe genetic drift and an extremely high level of inbreeding, as supported by low heterozygosity found across the genome. Detrimental effects of inbreeding depression are evident as cephalic malformations observed in all captured lizards of La Canna and might represent the more immediate threat to the persistence of this population.

A high-quality reference genome for the critically endangered Aeolian wall lizard, Podarcis raffonei.

The Aeolian wall lizard, Podarcis raffonei, is an endangered species endemic to the Aeolian archipelago, Italy, where it is present only in 3 tiny islets and a narrow promontory of a larger island. Because of the extremely limited area of occupancy, severe population fragmentation and observed decline, it has been classified as Critically Endangered by the International Union for the Conservation of Nature (IUCN). Using Pacific Biosciences (PacBio) High Fidelity (HiFi) long-read sequencing, Bionano optical mapping and Arima chromatin conformation capture sequencing (Hi-C), we produced a high-quality, chromosome-scale reference genome for the Aeolian wall lizard, including Z and W sexual chromosomes. The final assembly spans 1.51 Gb across 28 scaffolds with a contig N50 of 61.4 Mb, a scaffold N50 of 93.6 Mb, and a BUSCO completeness score of 97.3%. This genome constitutes a valuable resource for the species to guide potential conservation efforts and more generally for the squamate reptiles that are underrepresented in terms of available high-quality genomic resources.

Condition- and context-dependent variation of sexual dimorphism across lizard populations at different spatial scales.

The evolution of sexual dimorphism (SD) is driven by intricate interplays between sexual and natural selection. When it comes to SD variation within populations, however, environmental factors play a major role. Sexually selected traits are expected to be strongly dependent on individual body condition, which is influenced by the local environment that individuals experience. As a consequence, the degree of SD may also depend on resource availability. Here, we investigated the potential drivers of SD expression at two sexually dimorphic morphometric traits, body size (snout vent length) and head shape (head geometric morphometrics), in the Italian wall lizard (Podarcis siculus). We assessed the existence of condition- and context-dependent SD across ten islands of the Aeolian archipelago (southern Italy), at within- and among-population scales. We observed strong geographical variation of SD among islands, and tested three potential SD predictors related to resource availability (individual body condition, ecosystem productivity, temperature). Body condition and ecosystem productivity were the main drivers of body size SD variation, and body condition was also the main driver for head shape SD. Our results highlight that the expression of SD in the Italian wall lizard is both condition- and context-dependent. These results are congruent at within- and among-populations scales highlighting that spatial multi-scale analysis represents a useful approach to understand patterns of SD expression.

Population genetic differentiation and genomic signatures of adaptation to climate in an abundant lizard.

Species distributed across climatic gradients will typically experience spatial variation in selection, but gene flow can prevent such selection from causing population genetic differentiation and local adaptation. Here, we studied genomic variation of 415 individuals across 34 populations of the common wall lizard (Podarcis muralis) in central Italy. This species is highly abundant throughout this region and populations belong to a single genetic lineage, yet there is extensive phenotypic variation across climatic regimes. We used redundancy analysis to, first, quantify the effect of climate and geography on population genomic variation in this region and, second, to test if climate consistently sorts specific alleles across the landscape. Climate explained 5% of the population genomic variation across the landscape, about half of which was collinear with geography. Linear models and redundancy analyses identified loci that were significantly differentiated across climatic regimes. These loci were distributed across the genome and physically associated with genes putatively involved in thermal tolerance, regulation of temperature-dependent metabolism and reproductive activity, and body colouration. Together, these findings suggest that climate can exercise sufficient selection in lizards to promote genetic differentiation across the landscape in spite of high gene flow.

Population Genomics of Wall Lizards Reflects the Dynamic History of the Mediterranean Basin.

The Mediterranean Basin has experienced extensive change in geology and climate over the past six million years. Yet, the relative importance of key geological events for the distribution and genetic structure of the Mediterranean fauna remains poorly understood. Here, we use population genomic and phylogenomic analyses to establish the evolutionary history and genetic structure of common wall lizards (Podarcis muralis). This species is particularly informative because, in contrast to other Mediterranean lizards, it is widespread across the Iberian, Italian, and Balkan Peninsulas, and in extra-Mediterranean regions. We found strong support for six major lineages within P. muralis, which were largely discordant with the phylogenetic relationship of mitochondrial DNA. The most recent common ancestor of extant P. muralis was likely distributed in the Italian Peninsula, and experienced an "Out-of-Italy" expansion following the Messinian salinity crisis (∼5 Mya), resulting in the differentiation into the extant lineages on the Iberian, Italian, and Balkan Peninsulas. Introgression analysis revealed that both inter- and intraspecific gene flows have been pervasive throughout the evolutionary history of P. muralis. For example, the Southern Italy lineage has a hybrid origin, formed through admixture between the Central Italy lineage and an ancient lineage that was the sister to all other P. muralis. More recent genetic differentiation is associated with the onset of the Quaternary glaciations, which influenced population dynamics and genetic diversity of contemporary lineages. These results demonstrate the pervasive role of Mediterranean geology and climate for the evolutionary history and population genetic structure of extant species.

Prevalence of Gastrointestinal Symptoms in Severe Acute Respiratory Syndrome Coronavirus 2 Infection: Results of the Prospective Controlled Multinational GI-COVID-19 Study.

INTRODUCTION: Gastrointestinal (GI) symptoms in coronavirus-19 disease (COVID-19) have been reported with great variability and without standardization. In hospitalized patients, we aimed to evaluate the prevalence of GI symptoms, factors associated with their occurrence, and variation at 1 month. METHODS: The GI-COVID-19 is a prospective, multicenter, controlled study. Patients with and without COVID-19 diagnosis were recruited at hospital admission and asked for GI symptoms at admission and after 1 month, using the validated Gastrointestinal Symptom Rating Scale questionnaire. RESULTS: The study included 2036 hospitalized patients. A total of 871 patients (575 COVID+ and 296 COVID-) were included for the primary analysis. GI symptoms occurred more frequently in patients with COVID-19 (59.7%; 343/575 patients) than in the control group (43.2%; 128/296 patients) (P < 0.001). Patients with COVID-19 complained of higher presence or intensity of nausea, diarrhea, loose stools, and urgency as compared with controls. At a 1-month follow-up, a reduction in the presence or intensity of GI symptoms was found in COVID-19 patients with GI symptoms at hospital admission. Nausea remained increased over controls. Factors significantly associated with nausea persistence in COVID-19 were female sex, high body mass index, the presence of dyspnea, and increased C-reactive protein levels. DISCUSSION: The prevalence of GI symptoms in hospitalized patients with COVID-19 is higher than previously reported. Systemic and respiratory symptoms are often associated with GI complaints. Nausea may persist after the resolution of COVID-19 infection.

Multilocus Phylogeography of the Tuber mesentericum Complex Unearths Three Highly Divergent Cryptic Species.

Tuber mesentericum is an edible European black truffle, apparently easy to recognize, but showing a high degree of genetic variability. In this study, we performed an integrative taxonomic assessment of the T. mesentericum complex, combining a multilocus phylogeographic approach with morphological analyses, and including authentic specimens of Vittadini, and Berkeley and Broome. We performed maximum likelihood phylogenetic analyses, based on single and concatenated gene datasets (ITS rDNA, ß-tubulin, elongation factor 1-α), and including all available sequences from previous studies. Phylogenetic analyses consistently recovered three reciprocally monophyletic and well-supported clades: clade I, with a wide range across Europe; clade II, specimens collected mainly in the Iberian, Italian, and Balkan peninsulas; and clade III, specimens collected almost exclusively in central Italy. Genetic distance between clades ranged from 10.4% to 13.1% at the ITS region. We also designed new primer pairs specific for each phylogenetic lineage. Morphology of spores, asci, and peridium were investigated on specimens representing the three lineages. Macro- and micromorphological analyses of ascomata revealed only a few, but not diagnostic, differences between the three phylogenetic lineages, thus, confirming that they are morphologically cryptic. By studying authentic specimens of Vittadini, and Berkeley and Broome, it was possible to identify the three clades as T. mesentericum, Tuber bituminatum, and Tuber suave sp. nov., and to designate an epitype for T. mesentericum s.s. and a lectotype for T. bituminatum. Future investigations on volatile organic compound (VOC) composition are needed to define the aroma repertoires in this species complex.

Climate change effects on desert ecosystems: A case study on the keystone species of the Namib Desert Welwitschia mirabilis.

Deserts have been predicted to be one of the most responsive ecosystems to global climate change. In this study, we examine the spatial and demographic response of a keystone endemic plant of the Namib Desert (Welwitschia mirabilis), for which displacement and reduction of suitable climate has been foreseen under future conditions. The main aim is to assess the association between ongoing climate change and geographical patterns of welwitschia health, reproductive status, and size. We collected data on welwitschia distribution, health condition, reproductive status, and plant size in northern Namibia. We used ecological niche models to predict the expected geographic shift of suitability under climate change scenarios. For each variable, we compared our field measurements with the expected ongoing change in climate suitability. Finally, we tested the presence of simple geographical gradients in the observed patterns. The historically realized thermal niche of welwitschia will be almost completely unavailable in the next 30 years in northern Namibia. Expected reductions of climatic suitability in our study sites were strongly associated with indicators of negative population conditions, namely lower plant health, reduced recruitment and increased adult mortality. Population condition does not follow simple latitudinal or altitudinal gradients. The observed pattern of population traits is consistent with climate change trends and projections. This makes welwitschia a suitable bioindicator (i.e. a 'sentinel') for climate change effect in the Namib Desert ecosystems. Our spatially explicit approach, combining suitability modeling with geographic combinations of population conditions measured in the field, could be extensively adopted to identify sentinel species, and detect population responses to climate change in other regions and ecosystems.

Biogeographic and demographic history of the Mediterranean snakes Malpolon monspessulanus and Hemorrhois hippocrepis across the Strait of Gibraltar.

BACKGROUND: The contribution of North Africa to the assembly of biodiversity within the Western Palaearctic is still poorly documented. Since the Miocene, multiple biotic exchanges occurred across the Strait of Gibraltar, underlying the high biogeographic affinity between the western European and African sides of the Mediterranean basin. We investigated the biogeographic and demographic dynamics of two large Mediterranean-adapted snakes across the Strait and assess their relevance to the origin and diversity patterns of current European and North African populations. RESULTS: We inferred phylogeographic patterns and demographic history of M. monspessulanus and H. hippocrepis, based on range-wide multilocus data, combined with fossil data and species distribution modelling, under present and past bioclimatic envelopes. For both species we identified endemic lineages in the High Atlas Mountains (Morocco) and in eastern Iberia, suggesting their persistence in Europe during the Pleistocene. One lineage is shared between North Africa and southern Iberia and likely spread from the former to the latter during the sea-level low stand of the last glacial stage. During this period M. monspessulanus shows a sudden demographic expansion, associated with increased habitat suitability in North Africa. Lower habitat suitability is predicted for both species during interglacial stages, with suitable areas restricted to coastal and mountain ranges of Iberia and Morocco. Compiled fossil data for M. monspessulanus show a continuous fossil record in Iberia at least since the Pliocene and throughout the Pleistocene. CONCLUSIONS: The previously proposed hypothesis of Pleistocene glacial extinction of both species in Europe is not supported based on genetic data, bioclimatic envelopes models, and the available fossil record. A model of range retraction to mountain refugia during arid periods and of glacial expansion (demographic and spatial) associated to an increase of Mediterranean habitats during glacial epochs emerges as a general pattern for mesic vertebrates in North Africa. Moreover, the phylogeographic pattern of H. hippocrepis conforms to a well-established biogeographic partition between western and eastern Maghreb.

Climate Shapes the Geographic Distribution and Introgressive Spread of Color Ornamentation in Common Wall Lizards.

AbstractClimate can exert an effect on the strength of sexual selection, but empirical evidence is limited. Here, we tested whether climate predicts the geographic distribution and introgressive spread of sexually selected male color ornamentation across 114 populations of the common wall lizard, Podarcis muralis. Coloration was highly structured across the landscape and did not reflect genetic differentiation. Instead, color ornamentation was consistently exaggerated in hot and dry environments, suggesting that climate-driven selection maintains geographic variation in spite of gene flow. Introgression of color ornamentation into a distantly related lineage appears to be ongoing and was particularly pronounced in warm climates with wet winters and dry summers. Combined, these results suggest that sexual ornamentation is consistently favored in climates that allow a prolonged reproductive season and high and reliable opportunities for lizard activity. This pattern corroborates theoretical predictions that such climatic conditions reduce the temporal clustering of receptive females and increase male-male competition, resulting in strong sexual selection. In summary, we provide compelling evidence for the importance of climate for the evolution of color ornamentation, and we demonstrate that geographic variation in the strength of sexual selection influences introgression of this phenotype.

Molecular and morphological systematics of a new, reef forming, cupped oyster from the northern Arabian Gulf: Talonostrea salpinx new species.

The rocky northern shores of Kuwait and those of the western, inner shores of Kuwait Bay are dominated by a small, densely encrusting oyster. The identity of this oyster has never been confirmed and was mistaken previously for a small Saccostrea. The shell morphology suggests that this species belongs to the subfamily Crassostreinae, but within that subfamily, the presence of marginal erect trumpet-shaped projections is so far unique. Phylogenetic analyses based on mitochondrial DNA sequence data confirmed that this species belongs to the Crassostreinae and has a sister position to the clade including Talonostrea talonata and T. zhanjiangensis. Genetic distance between this species and Talonostrea species is remarkably high, being ~20% for the cytochrome oxidase I gene and ~7% for the 16S rRNA gene. Based on morphological and molecular analyses, this oyster is therefore described here as Talonostrea salpinx Oliver, Salvi & Al-Kandari, sp. nov. Shell morphology is shown to be variable, and the different forms encountered are described. The wider distribution and origins of this species, whether native or introduced, are discussed.

Status of the largest extant population of the critically endangered Aeolian lizard Podarcis raffonei (Capo Grosso, Vulcano island).

The Aeolian wall lizard Podarcis raffonei is an island endemic that survives only on three tiny islets, and on the Capo Grosso peninsula of the Vulcano island, thus is among the European vertebrates with the smallest range and one of the most threatened by extinction. This species is declining due to competition and hybridization with the non-native lizard Podarcis siculus, but a regular monitoring program is lacking. Here we assessed the size and status of the Capo Grosso population of P. raffonei on Vulcano. In September 2015 we captured 30 individuals showing the typical brown phenotype of P. raffonei, while one single male showed a green phenotype, apparently intermediate between P. raffonei and the non-native Podarcis siculus. In May 2017, only 47% of 131 individuals showed the typical brown phenotype (P. raffonei-like) and 53% showed the green phenotype (P. siculus-like). Based on N-mixture models and removal sampling the estimated size of the Capo Grosso population was of 800-1300 individuals in 2017, being similar to 2015; available data suggest that the total range of the species could be as small as 2 ha. The frequency of individuals with the typical P. raffonei phenotype dramatically dropped between two samplings with a parallel increase of individuals displaying the green phenotype. Observation on outdoor captive-bred individuals demonstrates plasticity for colouration in P. raffonei individuals from Capo Grosso, with several individuals showing the typical brown pattern in September 2017 and a green pattern in March 2021. Non-exclusive hypotheses, including hybridization with P. siculus and plasticity in colour pattern of P. raffonei, are discussed to explain the phenotypic shifts of the P. raffonei population of Capo Grosso. While genomic evidence is required to reach conclusions and investigate eventual hybridization, it is urgent to undertake a programme for the monitoring and management of this lizard.

Extensive introgression and mosaic genomes of Mediterranean endemic lizards.

The Mediterranean basin is a hotspot of biodiversity, fuelled by climatic oscillation and geological change over the past 20 million years. Wall lizards of the genus Podarcis are among the most abundant, diverse, and conspicuous Mediterranean fauna. Here, we unravel the remarkably entangled evolutionary history of wall lizards by sequencing genomes of 34 major lineages covering 26 species. We demonstrate an early (>11 MYA) separation into two clades centred on the Iberian and Balkan Peninsulas, and two clades of Mediterranean island endemics. Diversification within these clades was pronounced between 6.5-4.0 MYA, a period spanning the Messinian Salinity Crisis, during which the Mediterranean Sea nearly dried up before rapidly refilling. However, genetic exchange between lineages has been a pervasive feature throughout the entire history of wall lizards. This has resulted in a highly reticulated pattern of evolution across the group, characterised by mosaic genomes with major contributions from two or more parental taxa. These hybrid lineages gave rise to several of the extant species that are endemic to Mediterranean islands. The mosaic genomes of island endemics may have promoted their extraordinary adaptability and striking diversity in body size, shape and colouration, which have puzzled biologists for centuries.

Fossil-calibrated time tree of Podarcis wall lizards provides limited support for biogeographic calibration models.

Podarcis wall lizards are endemic to the Mediterranean Basin where they represent the predominant reptile group. Despite being extensively used as model organisms in evolutionary and ecological studies their phylogeny and historical biogeography are still incompletely resolved. Moreover, molecular clock calibrations used in wall lizard phylogeography are based on the assumption of vicariant speciation triggered by the abrupt Mediterranean Sea level rise at the end of the Messinian salinity crisis (MSC). However, the validity of this biogeographic calibration remains untested. In this study we inferred a robust time tree based on multilocus data and fossil calibrations using both gene concatenation and species-tree approaches and including models with gene-flow. We found five deeply divergent, geographically coherent, and well-supported clades comprising species from i) Iberian Peninsula and North Africa; ii) Western Mediterranean islands, iii) Sicilian and Maltese islands; and iv-v) Balkan region and Aegean islands. The mitochondrial tree shows some inconsistencies with the species tree that warrant future investigation. Diversification of main clades is estimated in a short time frame during the Middle Miocene and might have been associated with a period of global climate cooling with the establishment of a marked climatic zonation in Europe. Cladogenetic events within the main clades are scattered throughout the time tree, from the Late Miocene to the Early Pleistocene, suggesting that speciation events in wall lizards reflect a complex interplay between regional topography, climate and geological history rather than a shared major climatic or paleogeographic event. Our absolute time estimates, as well as a relative dating approach, demonstrate that the assumption of a causal link between sea-level rise at the end of the MSC and the diversification of many island endemics is not justified. This study reinforces the notion that multiple dispersal and vicariant events, at different time frames, are required to explain current allopatric distributions and to account for the historical assembly of Mediterranean biota, and cautions against the use of biogeographic calibrations based on the assumption of vicariance.

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.