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The joint expression of particular colors, morphologies, and behaviors is a common feature of adaptation, but the genetic basis for such "phenotypic syndromes" remains poorly understood. Here, we identified a complex genetic architecture associated with a sexually selected syndrome in common wall lizards, by capitalizing on the adaptive introgression of coloration and morphology into a distantly related lineage. Consistent with the hypothesis that the evolution of phenotypic syndromes in vertebrates is facilitated by developmental linkage through neural crest cells, most of the genes associated with the syndrome are involved in neural crest cell regulation. A major locus was a ~400-kb region, characterized by standing structural genetic variation and previously implied in the evolutionary innovation of coloration and beak size in birds. We conclude that features of the developmental and genetic architecture contribute to maintaining trait integration, facilitating the extensive and rapid introgressive spread of suites of sexually selected characters.

The Mediterranean lizard Podarcis lilfordi is an emblematic species of the Balearic Islands. The extensive phenotypic diversity among extant isolated populations makes the species a great insular model system for eco-evolutionary studies, as well as a challenging target for conservation management plans. Here we report the first high-quality chromosome-level assembly and annotation of the P. lilfordi genome, along with its mitogenome, based on a mixed sequencing strategy (10X Genomics linked reads, Oxford Nanopore Technologies long reads and Hi-C scaffolding) coupled with extensive transcriptomic data (Illumina and PacBio). The genome assembly (1.5 Gb) is highly contiguous (N50 = 90 Mb) and complete, with 99% of the sequence assigned to candidate chromosomal sequences and >97% gene completeness. We annotated a total of 25,663 protein-coding genes translating into 38,615 proteins. Comparison to the genome of the related species Podarcis muralis revealed substantial similarity in genome size, annotation metrics, repeat content, and a strong collinearity, despite their evolutionary distance (~18-20 MYA). This genome expands the repertoire of available reptilian genomes and will facilitate the exploration of the molecular and evolutionary processes underlying the extraordinary phenotypic diversity of this insular species, while providing a critical resource for conservation genomics., (© The Author(s) 2023. Published by Oxford University Press on behalf of Kazusa DNA Research Institute.)

Rapid technological improvements are democratizing access to high quality, chromosome-scale genome assemblies. No longer the domain of only the most highly studied model organisms, now non-traditional and emerging model species can be genome-enabled using a combination of sequencing technologies and assembly software. Consequently, old ideas built on sparse sampling across the tree of life have recently been amended in the face of genomic data drawn from a growing number of high-quality reference genomes. Arguably the most valuable are those long-studied species for which much is already known about their biology; what many term emerging model species. Here, we report a highly complete chromosome-scale genome assembly for the brown anole, Anolis sagrei - a lizard species widely studied across a variety of disciplines and for which a high-quality reference genome was long overdue. This assembly exceeds the vast majority of existing reptile and snake genomes in contiguity (N50 = 253.6 Mb) and annotation completeness. Through the analysis of this genome and population resequence data, we examine the history of repetitive element accumulation, identify the X chromosome, and propose a hypothesis for the evolutionary history of fusions between autosomes and the X that led to the sex chromosomes of A. sagrei., (© 2022. The Author(s).)

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., (© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)

Diversifications often proceed along highly conserved, evolutionary trajectories. These patterns of covariation arise in ontogeny, which raises the possibility that adaptive morphologies are biased towards trait covariations that resemble growth trajectories. Here, we test this prediction in the diverse clade of Anolis lizards by investigating the covariation of embryonic growth of 13 fore- and hindlimb bones in 15 species, and compare these to the evolutionary covariation of these limb bones across 267 Anolis species. Our results demonstrate that species differences in relative limb length are established already at hatching, and are resulting from both differential growth and differential sizes of cartilaginous anlagen. Multivariate analysis revealed that Antillean Anolis share a common ontogenetic allometry that is characterized by positive allometric growth of the long bones relative to metapodial and phalangeal bones. This major axis of ontogenetic allometry in limb bones deviated from the major axis of evolutionary allometry of the Antillean Anolis and the two clades of mainland Anolis lizards. These results demonstrate that the remarkable diversification of locomotor specialists in Anolis lizards are accessible through changes that are largely independent from ontogenetic growth trajectories, and therefore likely to be the result of modifications that manifest at the earliest stages of limb development.

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.

Anolis lizards originated in continental America but have colonized the Greater Antillean islands and recolonized the mainland, resulting in three major groups (Primary and Secondary Mainland and Greater Antillean). The adaptive radiation in the Greater Antilles has famously resulted in the repeated evolution of ecomorphs. Yet, it remains poorly understood to what extent this island radiation differs from diversification on the mainland. Here, we demonstrate that the evolutionary modularity between girdles and limbs is fundamentally different in the Greater Antillean and Primary Mainland Anolis. This is consistent with ecological opportunities on islands driving the adaptive radiation along distinct evolutionary trajectories. However, Greater Antillean Anolis share evolutionary modularity with the group that recolonized the mainland, demonstrating a persistent phylogenetic inertia. A comparison of these two groups support an increased morphological diversity and faster and more variable evolutionary rates on islands. These macroevolutionary trends of the locomotor skeleton in Anolis illustrate that ecological opportunities on islands can have lasting effects on morphological diversification.

Plasticity can put evolution on repeat if development causes species to generate similar morphologies in similar environments. Anolis lizards offer the opportunity to put this role of developmental plasticity to the test. Following colonization of the four Greater Antillean islands, Anolis lizards independently and repeatedly evolved six ecomorphs adapted to manoeuvring different microhabitats. By quantifying the morphology of the locomotor skeleton of 95 species, we demonstrate that ecomorphs on different islands have diverged along similar trajectories. However, microhabitat-induced morphological plasticity differed between species and did not consistently improve individual locomotor performance. Consistent with this decoupling between morphological plasticity and locomotor performance, highly plastic features did not show greater evolvability, and plastic responses to microhabitat were poorly aligned with evolutionary divergence between ecomorphs. The locomotor skeleton of Anolis may have evolved within a subset of possible morphologies that are highly accessible through genetic change, enabling adaptive convergence independently of plasticity., Competing Interests: NF, IJ, KM, RR, TU No competing interests declared, (© 2020, Feiner et al.)

Hybrid zones provide insights into the evolution of reproductive isolation. Sexual selection can contribute to the evolution of reproductive barriers, but it remains poorly understood how sexual traits impact gene flow in secondary contact. Here, we show that a recently evolved suite of sexual traits that function in male-male competition mediates gene flow between two lineages of wall lizards (Podarcis muralis). Gene flow was relatively low and asymmetric in the presence of exaggerated male morphology and coloration compared to when the lineages share the ancestral phenotype. Putative barrier loci were enriched in genomic regions that were highly differentiated between the two lineages and showed low concordance between the transects. The exception was a consistently low genetic exchange around ATXN1, a gene that modulates social behavior. We suggest that this gene may contribute to the male mate preferences that are known to cause lineage-assortative mating in this species. Although female choice modulates the degree of reproductive isolation in a variety of taxa, wall lizards demonstrate that both male-male competition and male mate choice can contribute to the extent of gene flow between lineages., (© 2020 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution.)

The radiation of Anolis lizards in the Caribbean is associated with a diversification of the functional match between morphology, habitat use, and locomotor performance. It has been hypothesized that the microhabitat a lizard is reared in can achieve a similar fit of form and function within a species. This predicts that plasticity in the locomotor apparatus is accompanied by changes in perching behavior or improved locomotor performance. To test this, we raised juveniles of two species (Anolis sagrei and Anolis carolinensis) on either broad or narrow surfaces and examined perching behavior and locomotor performance as well as the shape of the pectoral and pelvic girdles, limb length, and thickness of the long bones. Perching behavior was not affected by the habitat surface experienced during ontogeny. However, individuals raised on broad surfaces showed better locomotor performance on broad surfaces, and the magnitude of the effect was as large as the difference between the two species. Both species showed modifications of pectoral and pelvic shape, but only A. carolinensis developed longer limbs on broad surfaces. However, these morphological adjustments induced by physical activity did not explain why lizards raised on broad surfaces performed better. Thus, it appears that early-life experiences can affect both the morphology of the locomotor apparatus and locomotor performance in Anolis lizards, without the two being functionally connected., (© 2020 The Authors. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology published by Wiley Periodicals, Inc.)

Parasites have evolved a diversity of lifestyles that exploit the biology of their hosts. Some nematodes that parasitize mammals pass via the placenta or milk from one host to another. Similar cases of vertical transmission have never been reported in avian and nonavian reptiles, suggesting that egg laying may constrain the means of parasite transmission. However, here we report the first incidence of transovarial transmission of a previously undescribed nematode in an egg-laying amniote, the common wall lizard ( Podarcis muralis ). Nematodes enter the developing brain from the female ovary early in embryonic development. Infected lizard embryos develop normally and hatch with nematodes residing in their braincase. We present a morphological and molecular phylogenetic characterization of the nematode and suggest that particular features of lizard biology that are absent from birds and turtles facilitated the evolutionary origin of this novel life history.

Hox genes are a remarkable example of conservation in animal development and their nested expression along the head-to-tail axis orchestrates embryonic patterning. Early in vertebrate history, two duplications led to the emergence of four Hox clusters (A-D) and redundancy within paralog groups has been partially accommodated with gene losses. Here we conduct an inventory of squamate Hox genes using the genomes of 10 lizard and 7 snake species. Although the HoxC1 gene has been hypothesized to be lost in the amniote ancestor, we reveal that it is retained in lizards. In contrast, all snakes lack functional HoxC1 and -D12 genes. Varying levels of degradation suggest differences in the process of gene loss between the two genes. The vertebrate HoxC1 gene is prone to gene loss and its functional domains are more variable than those of other Hox1 genes. We describe for the first time the HoxC1 expression patterns in tetrapods. HoxC1 is broadly expressed during development in the diencephalon, the neural tube, dorsal root ganglia, and limb buds in two lizard species. Our study emphasizes the value of revisiting Hox gene repertoires by densely sampling taxonomic groups and its feasibility owing to growing sequence resources in evaluating gene repertoires across taxa., (© 2019 Wiley Periodicals, Inc.)

Reptiles use pterin and carotenoid pigments to produce yellow, orange, and red colors. These conspicuous colors serve a diversity of signaling functions, but their molecular basis remains unresolved. Here, we show that the genomes of sympatric color morphs of the European common wall lizard ( Podarcis muralis ), which differ in orange and yellow pigmentation and in their ecology and behavior, are virtually undifferentiated. Genetic differences are restricted to two small regulatory regions near genes associated with pterin [ sepiapterin reductase ( SPR )] and carotenoid [ beta-carotene oxygenase 2 ( BCO2 )] metabolism, demonstrating that a core gene in the housekeeping pathway of pterin biosynthesis has been coopted for bright coloration in reptiles and indicating that these loci exert pleiotropic effects on other aspects of physiology. Pigmentation differences are explained by extremely divergent alleles, and haplotype analysis revealed abundant transspecific allele sharing with other lacertids exhibiting color polymorphisms. The evolution of these conspicuous color ornaments is the result of ancient genetic variation and cross-species hybridization., Competing Interests: The authors declare no conflict of interest., (Copyright © 2019 the Author(s). Published by PNAS.)

Many features of the development of reptiles are affected by temperature, but very little is known about how incubation temperature affects gene expression. Here, we provide a detailed case study of gene expression profiles in common wall lizard (Podarcis muralis) embryos developing at stressfully low (15°C) versus benign (24°C) temperature. For maximum comparability between the two temperature regimes, we selected a precise developmental stage early in embryogenesis defined by the number of somites. We used a split-clutch design and lizards from four different populations to evaluate the robustness of temperature-responsive gene expression profiles. Embryos incubated at stressfully low incubation temperature expressed on average 20% less total RNA than those incubated at benign temperatures, presumably reflecting lower rates of transcription at cool temperature. After normalizing for differences in total amounts of input RNA, we find that approximately 50% of all transcripts show significant expression differences between the two incubation temperatures. Transcripts with the most extreme changes in expression profiles are associated with transcriptional and translational regulation and chromatin remodeling, suggesting possible epigenetic mechanisms underlying acclimation of early embryos to cool temperature. We discuss our findings in light of current advances in the use of transcriptomic data to study how individuals acclimatize and populations adapt to thermal stress., (© 2018 Wiley Periodicals, Inc.)

Populations adapting independently to the same environment provide important insights into the repeatability of evolution at different levels of biological organization. In the 20th century, common wall lizards (Podarcis muralis) from southern and western Europe were introduced to England, north of their native range. Nonnative populations of both lineages have adapted to the shorter season and lower egg incubation temperature by increasing the absolute rate of embryonic development. Here, we tested if this adaptation is accompanied by signatures of directional selection in the transcriptomes of early embryos and, if so, if nonnative populations show adaptive convergence. Embryos from nonnative populations exhibited gene expression profiles consistent with directional selection following introduction, but different genes were affected in the two lineages. Despite this, the functional enrichment of genes that changed their expression following introduction showed substantial similarity between lineages, and was consistent with mechanisms that should promote developmental rate. Moreover, the divergence between nonnative and native populations was enriched for genes that were temperature-responsive in native populations. These results indicate that small populations are able to adapt to new climatic regimes, but the means by which they do so may largely be determined by founder effects and other sources of genetic drift., (© 2017 The Author(s). Evolution © 2017 The Society for the Study of Evolution.)

Transposable elements (TEs) are DNA sequences that can insert elsewhere in the genome and modify genome structure and gene regulation. The role of TEs in evolution is contentious. One hypothesis posits that TE activity generates genomic incompatibilities that can cause reproductive isolation between incipient species. This predicts that TEs will accumulate during speciation events. Here, I tested the prediction that extant lineages with a relatively high rate of speciation have a high number of TEs in their genomes. I sequenced and analysed the TE content of a marker genomic region (Hox clusters) in Anolis lizards, a classic case of an adaptive radiation. Unlike other vertebrates, including closely related lizards, Anolis lizards have high numbers of TEs in their Hox clusters, genomic regions that regulate development of the morphological adaptations that characterize habitat specialists in these lizards. Following a burst of TE activity in the lineage leading to extant Anolis, TEs have continued to accumulate during or after speciation events, resulting in a positive relationship between TE density and lineage speciation rate. These results are consistent with the prediction that TE activity contributes to adaptive radiation by promoting speciation. Although there was no evidence that TE density per se is associated with ecological morphology, the activity of TEs in Hox clusters could have been a rich source for phenotypic variation that may have facilitated the rapid parallel morphological adaptation to microhabitats seen in extant Anolis lizards., (© 2016 The Author(s).)