Biology subjects

Benitez-Alvarez, L.

Publications and source records attributed to Benitez-Alvarez, L..

7 recordsLinked to original sources

bioRxiv2025

Parallel genomic remodeling associated with independent terrestrialization events in arthropods

The repeated transition from aquatic to terrestrial environments (terrestrialization) has shaped the evolutionary trajectory of many animal lineages, yet the genomic basis of this ecological shift remains incompletely understood. Arthropods, with multiple independent terrestrialization events, provide a powerful system to investigate whether parallel genomic changes underlie adaptation to land. Here, we present a phylum-wide comparative phylogenomic analysis of 309 arthropod species representing aquatic and terrestrial lineages, using gene family evolutionary dynamics and directional selection analyses to uncover shared genomic strategies associated with life on land. We identified thousands of orthogroups showing parallel expansions or contractions across the three main lineages that colonized land (Arachnida, Myriapoda, and Hexapoda), of which a significant proportion also exhibited lineage-specific shifts in selective pressure. Functional enrichment of these orthogroups revealed functional convergence on processes such as oxidative stress response, transmembrane transport, energy metabolism, exoskeleton formation, and moulting regulation. Notably, parallel evolution in aquaporins, solute carriers, cytochrome P450s, superoxide dismutases, and heat shock proteins suggests that a conserved terrestrialization toolkit underlies independent colonization events. Additionally, parallel remodeling of key developmental and immune signaling pathways highlights the role of regulatory and structural innovations in adapting to terrestrial challenges. Our results provide the first large-scale genomic evidence of parallel molecular evolution driving arthropod terrestrialization and emphasize the power of comparative genomics to reveal shared solutions to ecological transitions across deep evolutionary timescales.

evolutionary biology↗

bioRxiv2025

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↗

bioRxiv2025

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↗

bioRxiv2025

Disentangling the evolutionary history of terrestrial planarians through phylogenomics

Triclads (Platyhelminthes, Tricladida) are found in marine, freshwater, and terrestrial habitats worldwide except Antarctica. Terrestrial planarians are grouped into the family Geoplanidae, which is subdivided into the subfamilies Geoplaninae, Bipaliinae, Rhynchodeminae, and Microplaninae. Some of these subfamilies result from taxonomic rearrangements based on molecular phylogenies inferred from a few molecular markers. However, the diagnosis of Rhynchodeminae was not aligned with the morphology of all its representatives. While the subfamilies are recovered as monophyletic in recent molecular phylogenies, robust hypotheses regarding the relationships between them remain unknown. In this study, we employ for the first time a phylogenomic framework to investigate the evolutionary relationships among the subfamilies, starting by obtaining the first transcriptomes for 15 species of terrestrial planarians. A total of 16 different datasets, comprising nearly two thousand single-copy genes inferred from transcriptomic data, were analyzed using various phylogenetic inference methods. We recovered, for the first time, a well-supported topology of phylogenetic relationships among Geoplanidae subfamilies, positioning Bipaliinae and Microplaninae as a clade sister to Rhynchodeminae + Geoplaninae. Internal relationships within the genus Microplana were not supported in our analyses. The subfamily Rhynchodeminae, represented in our phylogeny by species from the tribes Rhynchodemini and Caenoplanini, is re-diagnosed to align with previous taxonomic rearrangements. This study not only represents a significant step forward in the phylogenetic resolution of Geoplanidae but also provides important insights into the broader evolutionary dynamics shaping land planarian diversity. HighlightsO_LIFirst transcriptomes of multiple terrestrial planarians sequenced. C_LIO_LIFirst molecular phylogeny of terrestrial planarians at subfamily level based on transcriptomic data. C_LIO_LIHighly supported topology for phylogenetic interrelationship among terrestrial planarians subfamilies. C_LIO_LIUnclear interrelationships between species from the genus Microplana. C_LIO_LIThe subfamily Rhynchodeminae is re-diagnosed at the morphological level. C_LI

evolutionary biology↗

bioRxiv2024

A punctuated burst of massive genomic rearrangements by chromosome shattering and the origin of non-marine annelids

The genomic basis of cladogenesis and adaptive evolutionary change has intrigued biologists for decades. Here, we show that the tectonics of genome evolution in clitellates, a clade composed of most freshwater and all terrestrial species of the phylum Annelida, is characterised by extensive genome-wide scrambling that resulted in a massive loss of macrosynteny between marine annelids and clitellates. These massive rearrangements included the formation of putative neocentromeres with newly acquired transposable elements and preceded a further period of genome-wide reshaping events, potentially triggered by the loss of genes involved in genome stability and homeostasis of cell division. Notably, while these rearrangements broke short-range interactions observed between Hox genes in marine annelids, they were reformed as long-range interactions in clitellates. Our findings reveal extensive genomic reshaping in clitellates at both the linear (2D) and three-dimensional (3D) levels, suggesting that, unlike in other animal lineages where synteny conservation constrains structural evolution, clitellates exhibit a remarkable tolerance for chromosomal rearrangements. Our study thus suggests that the genomic landscape of Clitellata resulted from a rare burst of genomic changes that ended a long period of stability that persists across large phylogenetic distances.

evolutionary biology↗

bioRxiv2024

MATEdb2, a collection of high-quality metazoan proteomes across the Animal Tree of Life to speed up phylogenomic studies

Recent advances in high throughput sequencing have exponentially increased the number of genomic data available for animals (Metazoa) in the last decades, with high-quality chromosome-level genomes being published almost daily. Nevertheless, generating a new genome is not an easy task due to the high cost of genome sequencing, the high complexity of assembly, and the lack of standardized protocols for genome annotation. The lack of consensus in the annotation and publication of genome files hinders research by making researchers lose time in reformatting the files for their purposes but can also reduce the quality of the genetic repertoire for an evolutionary study. Thus, the use of transcriptomes obtained using the same pipeline as a proxy for the genetic content of species remains a valuable resource that is easier to obtain, cheaper, and more comparable than genomes. In a previous study, we presented the Metazoan Assemblies from Transcriptomic Ensembles database (MATEdb), a repository of high-quality transcriptomic and genomic data for the two most diverse animal phyla, Arthropoda and Mollusca. Here, we present the newest version of MATEdb (MATEdb2) that overcomes some of the previous limitations of our database: (1) we include data from all animal phyla where public data is available, (2) we provide gene annotations extracted from the original GFF genome files using the same pipeline. In total, we provide proteomes inferred from high-quality transcriptomic or genomic data for almost 1000 animal species, including the longest isoforms, all isoforms, and functional annotation based on sequence homology and protein language models, as well as the embedding representations of the sequences. We believe this new version of MATEdb will accelerate research on animal phylogenomics while saving thousands of hours of computational work in a plea for open, greener, and collaborative science.

evolutionary biology↗

bioRxiv2022

First molecular phylogeny of the freshwater planarian genus Girardia (Platyelminthes, Tricladida) unveils hidden taxonomic diversity and initiates resolution of its historical biogeography

The genus Girardia (Platyhelminthes: Tricladida) comprises several species of which some have spread from their original areas of distribution in the Americas to other parts of the globe. Due to great anatomical similarities between species, morphology-based phylogenetic analyses struggled to resolve the affinities between species and species-groups. This problem is exacerbated by the fact that populations of Girardia may show only asexual reproduction by fissiparity and, thus, do not exhibit a copulatory apparatus, which hampers taxonomic identification and extraction of phylogenetic characters. In the present work this problem has been resolved by constructing a molecular phylogeny of the genus. Although our samples do not include representatives of all known species, they cover a large part of the original distributional range of the genus Girardia. Our phylogenetic results suggest the presence of two main clades, which are genetically and karyologically highly differentiated. North and South American nominal G. tigrina actually constitute two sibling species that are not even closely related. The South American form is here described as a new species. The phylogenetic tree brings to light that Girardia arose on the South American portion of Gondwanaland, from which it, subsequently, dispersed to the Nearctic Region, probably more than once.

evolutionary biology↗