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Genome-wide barriers to gene flow reveal the genetic basis of viviparity evolution in a lizard.

Viviparity (live-bearing) is a major evolutionary transition repeatedly linked with ecological and evolutionary diversification throughout vertebrates. Live-bearing reproduction entails a novel suite of phenotypes and life history traits, but the genetic processes by which such a reproductive innovation evolves are unknown. Remarkable among amniotes, the common lizard (Zootoca vivipara) has extant oviparous (egg-laying) and viviparous lineages and a to-date unresolved history of parity mode emergence. This species represents an ideal model to reconstruct the evolutionary and genetic mechanisms of how viviparity arises. By analyzing whole genomes of individuals from across the species' distribution, we robustly show that viviparity evolved once. However, gene flow from oviparous to viviparous populations is found to be long-term and extensive, causing pronounced gene tree discordance. We inferred signals of selection for viviparity in many independent regions across the genome, and these were recruited over considerable time. Genomic barriers to gene flow between oviparity and viviparity were found genome wide. These are enriched for regions under selection for parity mode and for genes known to be involved in pregnancy and parturition in squamates and mammals. Further implicating their functional role in viviparity, we show that genes in genomic regions under selection and resisting gene flow are more highly expressed in the uterus of viviparous lizards during pregnancy. Our study demonstrates that viviparity in an amniote evolved by selection in the face of gene flow and primarily by the genome-wide accumulation of functional regulatory variants. These results reveal how complex adaptive innovations can arise and be maintained.

Animals

Genome-Wide Mining of lncRNAs Reveals Their Potential Regulatory Role in the Evolution of Viviparity.

Reproduction in vertebrates usually involves egg-laying (oviparity) or live-bearing (viviparity). Oviparity is the ancestral trait from which viviparity has independently evolved more than 100 times in squamate reptiles. This transition involves a series of physiological and structural changes, including the degeneration of eggshell and the evolution of a placenta and differences in the temporal and spatial expression patterns of some functional genes that drive the structural transformation. Long non-coding RNAs (lncRNAs) play important roles in the regulation of gene expression, yet it remains unclear whether they participate in gene expression shifts during the transition from oviparity to viviparity, and if so how. Therefore, we employ deep mining to identify novel lncRNAs of a closely related oviparous-viviparous pair of lizards (Phrynocephalus przewalskii and P. vlangalii). We construct cis- and trans-regulatory networks between lncRNAs and target genes using the transcriptomic data of oviduct or uteri tissues across reproductive periods. Results show that lncRNAs that regulate eggshell gland developmental genes in the oviparous lizard are lost or less expressed in the viviparous lizard. A number of lncRNAs involved in the regulation of placental development and embryo attachment in viviparous species have no orthologs in oviparous species, and others show little or no expression. Accordingly, lncRNAs may play important regulatory roles in the physiological and structural changes in the transition from oviparity to viviparity. These results open doors to the further elucidation of genetic regulatory networks.

Animals

Comparative Transcriptomic Analyses Identify Candidate Genes for Convergent Reproductive Shifts in a Bimodal Viviparous Amphibian.

Shifts in reproductive mode represent key evolutionary innovations that shape species' life histories and evolutionary trajectories. Species showing bimodal reproductive strategies with multiple independent origins offer a rare opportunity to gain insights into the adaptive processes and mechanisms underlying convergent traits. The fire salamander, Salamandra salamandra, is the only amphibian exhibiting intraspecific variation in reproductive mode across multiple independent reproductive shifts, enabling investigation of the transition between larviparity (females give birth to aquatic larvae) and pueriparity (females give birth to fully developed terrestrial juveniles) within a single species and across different timescales. Pueriparity is an adaptive innovation that skips the aquatic larval stage, allowing individuals to exploit habitats with no available water bodies. The fire salamander is larviparous across most of its range, but pueriparity has evolved independently at least three times: once in the early Pleistocene within S. s. bernardezi in the mountains of northern Spain, and more recently on two land-bridge islands (NW Spain) inhabited by S. s. gallaica. To identify candidate genes associated with these distinct reproductive modes, we compared gene expression profiles of the uterus and oviduct of pregnant females across two independent evolutionary transitions using RNA-sequencing. We detected shared changes in maternal gene expression among pueriparous S. s. bernardezi and S. s. gallaica relative to their larviparous counterparts, in addition to differences unique to each independent evolutionary transition. Functional enrichment analyses indicated that differentially expressed genes were associated with reproductive timing, angiogenesis, and maternal signalling, consistent with the phenotypic differences observed in the uterine environment and embryonic development between the two reproductive modes. This study represents an important first step towards understanding the genomic basis of the evolution of pueriparity in a remarkable bimodal reproductive system, and provides transcriptomic resources and candidate genes for future research into the genomic architecture underlying this poorly understood adaptive trait.

Animals

Chromosome-Level Reference Genome of the Desert Night Lizard Xantusia vigilis.

We present a reference-quality genome assembly for the desert night lizard (Xantusia vigilis). The night lizards (Xantusiidae) are a family of small-bodied lizards found in North America (Xantusia), Central America (Lepidophyma), and Cuba (Cricosaura). The night lizard family has an independent evolutionary history of at least 80 million years from its sister taxa within Scincoidea. The Xantusiids have several unique ecological, behavioral and evolutionary characteristics. For instance, the family contains the only squamate species that form diploid, unisexual, parthenogenic lineages. In addition, most night lizards are viviparous and form stable kin groups that are maintained over multiple years, an unusual life history strategy among lizards. Combining PacBio long-read sequencing, Hi-C, and RNAseq data we developed a reference-quality genome for the desert night lizard, X. vigilis. We assembled a complete mitochondrion and ~ 2.2 Gb nuclear genome, with 20 scaffolds that correlate in size to the X. vigilis karyotype. In addition, we found that X. vigilis chromosome 1 aligns with gene content of both of macrochromosome 1 and microchromosome 9 from a genome assembly of a species in the sister family Cordylidae (Hemicordylus capensis).

Xantusia

Evolutionary Conservation and Reproductive Expression of ABC Transporter Genes in Two Sphenomorphus Skinks.

ATP-binding cassette (ABC) transporters represent one of the largest membrane protein superfamilies in vertebrates, playing essential roles in translocating diverse substrates across membranes. However, knowledge of ABC transporter genes in reptiles remains limited. In this study, we conducted a comprehensive genome-wide identification and characterization of the ABC gene family in oviparous Sphenomorphus incognitus and viviparous Sphenomorphus indicus. A total of 45 ABC genes were identified in each species and classified into seven subfamilies (ABCA-ABCG). Comparative and phylogenetic analyses revealed a generally conserved gene repertoire, with limited duplication events observed mainly in the ABCA and ABCG subfamilies, whereas other subfamilies (e.g., ABCE, ABCF, and ABCD) remained highly conserved. Interestingly, a lineage-specific duplication of ABCC2 was identified in lizards. Oviductal expression profiling revealed distinct temporal patterns of ABC gene expression across reproductive stages. Several genes, including ABCG1, ABCC3, and ABCD4, exhibited conserved expression trajectories across both species, suggesting shared transcriptional regulation. In contrast, ABCA1, ABCB1, and ABCG2 showed species-specific expression patterns, indicating regulatory divergence between the two lizard species. Overall, ABC gene expression was more dynamic in S. incognitus than in S. indicus. In summary, although the ABC transporter family is structurally conserved, it exhibits lineage-specific evolutionary changes and divergent transcriptional regulation in lizard oviducts. This study provides a foundation for understanding the diversity and regulation of ABC transporter genes in reptiles.

Animals

Tandem gene duplication facilitates intertidal adaptation in atypical mangrove plants.

Mangrove plants, originating from inland ancestors, have independently adapted to extreme intertidal zones characterized by salt and hypoxia stress. While typical mangroves exhibit specialized phenotypes, like viviparous seeds and salt secretion, atypical clades that have thrived without such traits are particularly suitable for exploring the molecular and physiological basis underlying plant adaptation to intertidal zones. We assembled a chromosome-level genome of an atypical mangrove, Scyphiphora hydrophylacea, the only mangrove species in Gentianales. Similar to other mangroves, S. hydrophylacea colonized intertidal zones during climatic optimum periods of sea-level rise. Despite lacking recent whole-genome duplications (WGDs), its genome acquired extensive tandem gene duplications (TDs), leading to the rapid expansion of key salt- and hypoxia-related genes. Transcriptome data further corroborated that TD-driven gene expansions contribute to stress tolerance. Specifically, the expansion of genes involved in cation transmembrane transport, osmotic regulation, and oxidative stress response may enhance salinity tolerance, and the expansion of signal transduction and energy metabolism genes in hypoxia-response pathways may confer waterlogging tolerance. Therefore, in the absence of large-scale gene duplication, the rapid expansion of core genes involved in salt and hypoxia tolerance through tandem duplication may represent a key force driving the adaptation of atypical mangroves. These findings also provide valuable insights for crop improvement strategies aimed at enhancing environmental resilience while maintaining phenotypic stability.

Gene Duplication