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Garcia-Vernet, R.

Publications and source records attributed to Garcia-Vernet, R..

3 recordsLinked to original sources

Independent genomic trajectories shape adaptation to life on land across animal lineages

How animals repeatedly adapted to life on land is a central question in evolutionary biology. While terrestrialisation occurred independently across animal phyla, it remains unclear whether shared genomic mechanisms underlie these transitions. Here, we combine large-scale comparative genomics, machine learning, and multi-omics data, including proteomics and transcriptomics from stress experiments relevant to terrestrial environmental challenges in 17 species, to investigate the genomic basis of animal terrestrial adaptation. Gene co-expression networks reveal that genes relevant to stress are largely lineage-specific, yet converge in function through the co-option of gene families pre-dating terrestrialisation events. Phylogenomic and machine learning analyses support a dominant role for early-evolving genes, enriched in stress-related functions, paired with a higher gene loss than gain at terrestrialisation nodes. Our findings support a model of lineage-specific genomic changes involving mostly conserved genes that converged at the functional level during the independent transitions to terrestrial life.

evolutionary biology↗

A proteo-transcriptomic investigation of toxin evolution in planarians and their role in flatworm terrestrialization

The transition from aquatic to terrestrial environments represents a major evolutionary transition in animals, requiring significant adaptations in physiology and defense mechanisms to the challenges presented by the harsh terrestrial environment. Platyhelminthes, which include both aquatic and terrestrial species with a single terrestrialization event in the family Geoplaniidae, serve as excellent model organisms for studying the evolutionary adaptations required for terrestrialization. This study investigates the evolutionary dynamics of toxin orthologous groups (as a proxy to gene families) in aquatic and terrestrial flatworms, together with mucus composition, focusing on their role in terrestrialization from a molecular ecology perspective. Using a proteo-transcriptomic approach, we predicted and identified a broader toxin gene repertoire in terrestrial flatworms compared to freshwater ones. Although most toxins in flatworms arose before terrestrial planarian diversification--gaining a novel evolutionary origin at the Tricladida and Continenticola nodes--the mucus protein repertoire appears to have a far older evolutionary origin in both species. Moreover, distinct orthologous groups underpin the toxin gene repertoire and mucus composition in each lineage, highlighting the contrasting evolutionary trajectories of these two functional components. While toxin families in both aquatic and terrestrial flatworms revealed overall common functions, including cytokine modulation and ion channel regulation, terrestrial flatworms exhibited specific expansions of lectin-like proteins and pro-inflammatory responses, highlighting their potential key role to respond to land-based threats. This study provides new insights into the differential evolutionary trajectories of toxin and mucus proteins in planarians, offering a deeper understanding of the genetic innovations that facilitated flatworm terrestrialization.

evolutionary biology↗

Genomic exaptation and regulatory landscape shifts as key mechanisms enabling flatworm terrestrialization

Understanding the genomic toolkit that facilitated animal terrestrialization--the transition from aquatic to terrestrial environments--is crucial for unravelling the evolutionary processes behind the origin and diversification of terrestrial biodiversity. Despite its significance, the genomic foundations driving the physiological and metabolic adaptations required for life on land remain largely unexplored across most terrestrial animal phyla. Planarians (phylum Platyhelminthes) represent an ideal model for studying terrestrialization, as only one terrestrial lineage, the family Geoplanidae (order Tricladida) is known to exist. Here, we used an integrative approach combining genomics, transcriptomics, and proteomics to investigate the genetic underpinnings potentially facilitating adaptation to terrestrial environments. Our analysis revealed a significant burst of gene gain preceding the diversification of terrestrial planarians and their split from freshwater relatives, in the branch leading to Tricladida. Upon exposure to abiotic stress, terrestrial and freshwater planarians exhibited distinct genetic toolkits: most differentially expressed genes emerged in orthologous groups gained specifically in the branch leading to Tricladida, over half of which showed signs of strong directional selection in terrestrial flatworms, indicating their adaptive importance for land colonization. Transcriptomic analyses further revealed contrasting stress responses: terrestrial planarians upregulated ancient genes whose origin predates the Geoplanidae lineage to cope with abiotic stress, while freshwater planarians downregulated a separate set of ancestral genes. Our genomic, transcriptomic, and proteomic data consistently show that the genetic toolkit for abiotic stress response in terrestrial planarians is highly differentiated from that of their freshwater counterparts, with significant regulatory shifts as well. Overall, our findings suggest a burst of gene gain in the Tricladida lineage, with co-option of these genes, rather than clade-specific innovations, playing a critical role in the origin and diversification of terrestrial flatworms. This underscores genomic exaptation and regulatory landscape shifts as key mechanisms enabling terrestrialization within Platyhelminthes. This study offers the first genome-wide insight into the genetic toolkit underlying flatworm terrestrialization and contributes broadly to understanding the genomic basis of animal terrestrialization.

evolutionary biology↗