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Feiner, N.

Publications and source records attributed to Feiner, N..

10 recordsLinked to original sources

Towards understanding the mechanistic basis of a sex-limited color polymorphism

The presence of multiple discrete color patterns within a species has captivated evolutionary biologists for more than a century, especially when such polymorphism is confined to one sex. The brown anole Anolis sagrei exhibits a female-limited polymorphism in dorsal patterning, which is controlled by allelic variation at the autosomal gene CCDC170. Here, we present and test a threshold model that can explain why the polymorphism is female-limited. We hypothesize that allelic variation at the CCDC170 locus affects only female color pattern because this gene is co-expressed with its neighboring gene ESR1, highly expressed in female, but not male, embryos. By manipulating embryonic estradiol levels, we show that genetic males can be induced to express the polymorphism according to allelic variation at the CCDC170 locus, which is naturally masked by low expression levels of this gene. Inversely, treating genetic females with fadrozole, which depletes estradiol, leads to monomorphic patterns irrespective of genotype, as for natural males. Using RT-qPCR, we demonstrate that these effects are accompanied by a direct influence of estradiol and fadrozole on gene expression levels of CCDC170 and ESR1, thereby validating the threshold model. Our results suggest that the CCDC170-ESR1-locus is part of a mechanistic link between the morph-determining and the sex differentiation systems and provide a causal explanation for the developmental origin of a sex-limited color polymorphism.

developmental biology↗

Neural crest cell biology shapes lizard skull evolution across evolutionary time scales

The vertebrate skull originates from two embryonic lineages, the mesoderm and the neural crest, offering a unique framework to study how developmental mechanisms connect phenotypic variation and evolutionary diversification. Using 3D geometric morphometrics, we analysed skull shape variation in lacertid lizards. Mesoderm- and neural crest-derived bones formed distinct, conserved modules at both micro- and macroevolutionary scales. In the common wall lizard (Podarcis muralis), rapid evolution of skull shape under sexual selection was primarily driven by neural crest-derived bones. While the primary axis of shape divergence in P. muralis aligned with a major axis of variation across lacertids, neural crest-derived bones exhibited slower evolutionary rates and lower morphological disparity than mesodermal-derived bones. We propose that this discrepancy between the role of the neural crest for skull evolution on micro- and macroevolution reflects constraints imposed by neural crest cell biology: although developmental plasticity enables rapid, correlated responses under sexual selection, pleiotropy may limit long-term evolvability of neural crest-derived skull regions. Teaser textThe bones of the vertebrate skull come from two developmental sources: the mesoderm and the neural crest. This dual origin allows to study how development influences evolution. Using 3D models of lizard skulls--including a species with exaggerated male traits linked to the neural crest--we examined patterns of skull variation. We found that neural crest-derived bones contribute to rapid changes driven by sexual selection. However, across different species, these same skull regions evolve more slowly and show less variation. This suggests that while neural crest cells may constrain long-term evolution because of their wide influence, they can also enable fast adaptations. The developmental biology of a trait therefore shapes its evolution.

evolutionary biology↗

Enrichment of neural crest cells by antibody labelling and flow cytometry for single-cell transcriptomics in a lizard

Neural crest cells (NCCs) are a key component of the vertebrate body plan and contribute to a variety of different traits. However, their dynamic migratory behavior and spatiotemporal heterogeneity in the developing embryo pose significant challenges for their identification and isolation. Consequently, most studies of NCCs have been confined to model organisms with established transgenic tools. To overcome this limitation, we present a novel approach that combines antibody labelling with fluorescence activated cell sorting to enrich for NCCs and we demonstrate the approach in the common wall lizard (Podarcis muralis). Through microscopy, reverse transcription quantitative polymerase chain reaction and single-cell RNA sequencing, we show that the method enriches for NCCs as efficiently as methods relying on transgenic animals. Using this technique, we successfully characterise transcriptional profiles of NCCs in wall lizard embryos. We anticipate that this method can be applied to a wide range of vertebrates that lack transgenic tools, enabling deeper insights into the roles that neural crest cells are playing in developmental and evolution.

developmental biology↗

Spatiotemporal profiling of neural crest cells in the common wall lizard Podarcis muralis

BackgroundNeural crest cells (NCCs) are migratory embryonic stem cells that give rise to a diverse set of cell types. Here we describe the dynamic distribution of NCCs in developing embryos of the common wall lizard Podarcis muralis inferred from ten markers. Our aim is to provide insights into the NCC development of lacertid lizards and to infer evolutionary modifications by comparisons to other tetrapods. ResultsNCC migration is ongoing at oviposition, following three streams in the head and multiple in the trunk. From 21ss, we observe expression patterns indicating the beginning of differentiation towards mesenchymal and neuronal fates. By 35ss, migration is restricted to caudal levels, and fully differentiated chromaffin cells are observed. ConclusionsWe find that some markers show patterns that differ from other tetrapods. For example, the antibody HNK-1 labels three NCC streams from the hindbrain while some comparable reptile studies describe four. However, the information emerging from all markers combined shows that the overall spatiotemporal distribution of NCCs in the common wall lizard is largely conserved with that of other tetrapods. Our study highlights the dynamic nature of seemingly canonical marker genes and provides the first description of spatiotemporal NCC dynamics in a lacertid lizard.

developmental biology↗

Chromosome-level genome assembly of Lilford's wall lizard, Podarcis lilfordi (Gunther, 1874) from the Balearic Islands (Spain)

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, assigning 72% to known functions. Comparison to the genome of the related species Podarcis muralis revealed substantial similarity in genome size, annotation metrics, repeat content, and 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.

genomics↗

Environmentally-induced DNA methylation is inherited across generations in an aquatic keystone species (Daphnia magna)

Environmental stress can result in epigenetic modifications that are passed down several generations. Such epigenetic inheritance can have significant impact on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. Here, we used whole-genome bisulfite sequencing on individual water fleas (Daphnia magna) to assess whether environmentally-induced DNA methylation can persist for up to four generations. Genetically identical females were exposed to a control treatment, one of three natural stressors (high temperature, zinc, microcystin), or the methylation-inhibitor 5-azacytidine. After exposure, lines were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) between controls and F1 individuals whose mothers (and therefore they themselves as germ cells) were exposed to one of the three natural stressors. Between 46% and 58% of these environmentally-induced DMPs persisted until generation F4 without attenuation in their magnitude of differential methylation. DMPs were enriched in exons and largely stressor-specific, suggesting a possible role in environment-dependent gene regulation. In contrast, treatment with the compound 5-azacytidine demonstrated that pervasive hypo-methylation upon exposure is reset almost completely after a single generation. These results suggest that environmentally-induced DNA methylation is non-random and stably inherited across generations in Daphnia, making epigenetic inheritance a putative factor in the eco-evolutionary dynamics of fresh-water communities. Author summaryWater fleas are important keystone species mediating eco-evolutionary dynamics in lakes and ponds. It is currently an open question in how far epigenetic inheritance contributes to the ability of Daphnia populations to adapt to environmental stress. Using a range of naturally occurring stressors and a multi-generational design, we show that environmentally-induced DNA methylation variants are stably inherited for at least four generations in Daphnia magna. The induced variation in DNA methylation are stressor-specific and almost exclusively found in exons, bearing the signatures of functional adaptations. Our findings imply that ecological adaptations of Daphnia to seasonal fluctuations can be underpinned by epigenetic inheritance of DNA methylation without changes in gene frequencies.

evolutionary biology↗

Chromosome-scale genome assembly of the brown anole (Anolis sagrei), a model species for evolution and ecology

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 new, 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.

genomics↗

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 flow 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.

evolutionary biology↗

Behavioural adaptations in egg laying ancestors facilitate evolutionary transitions to live birth

Live birth is a key innovation that has evolved from egg laying ancestors over 100 times in reptiles. However, egg-laying lizards and snakes often possess preferred body temperatures that are lethal to developing embryos, which should select against egg retention. Here, we demonstrate that thermal mismatches between mothers and offspring are widespread across the squamate phylogeny. This mismatch is resolved by gravid females adjusting their body temperature towards the thermal optimum of embryos. Importantly, phylogenetic reconstructions suggest this thermoregulatory behaviour evolved in egg-laying species prior to the evolution of live birth. Maternal thermoregulatory behaviour therefore bypasses the constraints imposed by a slowly evolving thermal physiology and has likely been a key facilitator in the repeated transitions to live birth.

evolutionary biology↗

Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard

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, 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 (SPR) and carotenoid metabolism (BCO2), demonstrating that a core gene in the housekeeping pathway of pterin biosynthesis has been co-opted 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 trans-specific 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.

evolutionary biology↗