Genomic Signatures of Domestication in a Fungus Obligately Farmed by Leafcutter Ants.

The naturally selected fungal crop (Leucoagaricus gongylophorus) farmed by leafcutter ants shows striking parallels with artificially selected plant crops domesticated by humans (e.g., polyploidy, engorged nutritional rewards, dependence on cultivation). To date, poorly resolved L. gongylophorus genome assemblies based on short-read sequencing have constrained hypotheses about how millions of years under cultivation by ants shaped the fungal crop genome and potentially drove domestication. We use PacBio HiFi sequencing of L. gongylophorus from the leafcutter ant Atta colombica to identify 18 putatively novel biosynthetic gene clusters that likely cemented life as a cultivar (e.g., plant fragment degradation, ant-farmer communication, antimicrobial defense). Comparative analyses with cultivated and free-living fungi showed genomic signatures of stepwise domestication transitions: 1) free-living to ant-cultivated: loss of genes conferring stress response and detoxification, 2) hyphal food to engorged nutritional rewards: expansions of genes governing cellular homeostasis, carbohydrate metabolism, and siderophore biosynthesis, and 3) detrital provisioning to freshly cut plant fragments: gene expansions promoting cell wall biosynthesis, fatty acid metabolism, and DNA repair. Comparisons across L. gongylophorus fungi farmed by three leafcutter ant species highlight genomic signatures of exclusively vertical clonal propagation and widespread transposable element activity. These results show how natural selection can shape domesticated cultivar genomes towards long-term ecological resilience of farming systems that have thrived across millennia.

GALEON: a comprehensive bioinformatic tool to analyse and visualize gene clusters in complete genomes.

MOTIVATION: Gene clusters, defined as a set of genes encoding functionally related proteins, are abundant in eukaryotic genomes. Despite the increasing availability of chromosome-level genomes, the comprehensive analysis of gene family evolution remains largely unexplored, particularly for large and highly dynamic gene families or those including very recent family members. These challenges stem from limitations in genome assembly contiguity, particularly in repetitive regions such as large gene clusters. Recent advancements in sequencing technology, such as long reads and chromatin contact mapping, hold promise in addressing these challenges. RESULTS: To facilitate the identification, analysis, and visualization of physically clustered gene family members within chromosome-level genomes, we introduce GALEON, a user-friendly bioinformatic tool. GALEON identifies gene clusters by studying the spatial distribution of pairwise physical distances among gene family members along with the genome-wide gene density. The pipeline also enables the simultaneous analysis and comparison of two gene families and allows the exploration of the relationship between physical and evolutionary distances. This tool offers a novel approach for studying the origin and evolution of gene families. AVAILABILITY AND IMPLEMENTATION: GALEON is freely available from https://www.ub.edu/softevol/galeon and https://github.com/molevol-ub/galeon.

The genomic basis of the plant island syndrome in Darwin's giant daisies.

The repeated, rapid and often pronounced patterns of evolutionary divergence observed in insular plants, or the 'plant island syndrome', include changes in leaf phenotypes, growth, as well as the acquisition of a perennial lifestyle. Here, we sequence and describe the genome of the critically endangered, Galápagos-endemic species Scalesia atractyloides Arnot., obtaining a chromosome-resolved, 3.2-Gbp assembly containing 43,093 candidate gene models. Using a combination of fossil transposable elements, k-mer spectra analyses and orthologue assignment, we identify the two ancestral genomes, and date their divergence and the polyploidization event, concluding that the ancestor of all extant Scalesia species was an allotetraploid. There are a comparable number of genes and transposable elements across the two subgenomes, and while their synteny has been mostly conserved, we find multiple inversions that may have facilitated adaptation. We identify clear signatures of selection across genes associated with vascular development, growth, adaptation to salinity and flowering time, thus finding compelling evidence for a genomic basis of the island syndrome in one of Darwin's giant daisies.

The First Genome of the Balearic Shearwater (Puffinus mauretanicus) Provides a Valuable Resource for Conservation Genomics and Sheds Light on Adaptation to a Pelagic lifestyle.

The Balearic shearwater (Puffinus mauretanicus) is the most threatened seabird in Europe and a member of the most speciose group of pelagic seabirds, the order Procellariiformes, which exhibit extreme adaptations to a pelagic lifestyle. The fossil record suggests that human colonisation of the Balearic Islands resulted in a sharp decrease of the Balearic shearwater population size. Currently, populations of the species continue to be decimated mainly due to predation by introduced mammals and bycatch in longline fisheries, with some studies predicting its extinction by 2070. Here, using a combination of short and long reads, we generate the first high-quality reference genome for the Balearic shearwater, with a completeness amongst the highest across available avian species. We used this reference genome to study critical aspects relevant to the conservation status of the species and to gain insights into the adaptation to a pelagic lifestyle of the order Procellariiformes. We detected relatively high levels of genome-wide heterozygosity in the Balearic shearwater despite its reduced population size. However, the reconstruction of its historical demography uncovered an abrupt population decline potentially linked to a reduction of the neritic zone during the Penultimate Glacial Period (∼194-135 ka). Comparative genomics analyses uncover a set of candidate genes that may have played an important role into the adaptation to a pelagic lifestyle of Procellariiformes, including those for the enhancement of fishing capabilities, night vision, and the development of natriuresis. The reference genome obtained will be the crucial in the future development of genetic tools in conservation efforts for this Critically Endangered species.

A high-quality genome assembly and annotation of the dark-eyed junco Junco hyemalis, a recently diversified songbird.

The dark-eyed junco (Junco hyemalis) is one of the most common passerines of North America, and has served as a model organism in studies related to ecophysiology, behavior, and evolutionary biology for over a century. It is composed of at least 6 distinct, geographically structured forms of recent evolutionary origin, presenting remarkable variation in phenotypic traits, migratory behavior, and habitat. Here, we report a high-quality genome assembly and annotation of the dark-eyed junco generated using a combination of shotgun libraries and proximity ligation Chicago and Dovetail Hi-C libraries. The final assembly is ∼1.03 Gb in size, with 98.3% of the sequence located in 30 full or nearly full chromosome scaffolds, and with a N50/L50 of 71.3 Mb/5 scaffolds. We identified 19,026 functional genes combining gene prediction and similarity approaches, of which 15,967 were associated to GO terms. The genome assembly and the set of annotated genes yielded 95.4% and 96.2% completeness scores, respectively when compared with the BUSCO avian dataset. This new assembly for J. hyemalis provides a valuable resource for genome evolution analysis, and for identifying functional genes involved in adaptive processes and speciation.

De novo transcriptome sequencing of the northern fowl mite, Ornithonyssus sylviarum, shed light on parasitiform poultry mites evolution and its chemoreceptor repertoires.

The northern fowl mite (NFM), Ornithonyssus sylviarum, and the poultry red mite (PRM), Dermanyssus gallinae, are the most serious pests of poultry, both of which have an expanding global prevalence. Research on NFM has been constrained by a lack of genomic and transcriptomic data. Here, we report and analyze the first global transcriptome data across all mite live stages and sexes. A total of 28,999 unigenes were assembled, of which 19,750 (68.10%) were annotated using seven functional databases. The biological function of these unigenes was classified using the GO, KOG, and KEGG databases. To gain insight into the chemosensory receptor-based system of parasitiform mites, we furthermore assessed the gene repertoire of gustatory receptors (GRs) and ionotropic receptors (IRs), both of which encode putative ligand-gated ion channel proteins. While these receptors are well characterized in insect model species, our understanding of chemosensory detection in mites and ticks is in its infancy. To address this paucity of data, we identified 9 IR/iGluRs and 2 GRs genes by analyzing transcriptome data in the NFM, while 9 GRs and 41 IR/iGluRs genes were annotated in the PRM genome. Taken together, the transcriptomic and genomic annotation of these two species provide a valuable reference for studies of parasitiform mites and also help to understand how chemosensory gene family expansion/contraction events may have been reshaped by an obligate parasitic lifestyle compared with their free-living closest relatives. Future studies should include additional species to validate this observation and functional characterization of the identified proteins as a step forward in identifying tools for controlling these poultry pests.

The chromosome-scale assembly of the Canary Islands endemic spider Dysdera silvatica (Arachnida, Araneae) sheds light on the origin and genome structure of chemoreceptor gene families in chelicerates.

Here, we present the chromosome-level genome assembly of Dysdera silvatica Schmidt, 1981, a nocturnal ground-dwelling spider endemic from the Canary Islands. The genus Dysdera has undergone a remarkable diversification in this archipelago mostly associated with shifts in the level of trophic specialization, becoming an excellent model to study the genomic drivers of adaptive radiations. The new assembly (1.37 Gb; scaffold N50 of 174.2 Mb), was performed using the chromosome conformation capture scaffolding technique, represents a continuity improvement of more than 4500 times with respect to the previous version. The seven largest scaffolds or pseudochromosomes, which cover 87% of the total assembly size, probably correspond with the seven chromosomes of the karyotype of this species, including a characteristic large X chromosome. To illustrate the value of this new resource we performed a comprehensive analysis of the two major arthropod chemoreceptor gene families (i.e., gustatory and ionotropic receptors). We identified 545 chemoreceptor sequences distributed across all pseudochromosomes, with a notable underrepresentation in the X chromosome. At least 54% of them localize in 83 genomic clusters with a significantly lower evolutionary distances between them than the average of the family, suggesting a recent origin of many of them. This chromosome-level assembly is the first high-quality genome representative of the Synspermiata clade, and just the third among spiders, representing a new valuable resource to gain insights into the structure and organization of chelicerate genomes, including the role that structural variants, repetitive elements and large gene families played in the extraordinary biology of spiders.

The Tetragnatha kauaiensis Genome Sheds Light on the Origins of Genomic Novelty in Spiders.

Spiders (Araneae) have a diverse spectrum of morphologies, behaviors, and physiologies. Attempts to understand the genomic-basis of this diversity are often hindered by their large, heterozygous, and AT-rich genomes with high repeat content resulting in highly fragmented, poor-quality assemblies. As a result, the key attributes of spider genomes, including gene family evolution, repeat content, and gene function, remain poorly understood. Here, we used Illumina and Dovetail Chicago technologies to sequence the genome of the long-jawed spider Tetragnatha kauaiensis, producing an assembly distributed along 3,925 scaffolds with an N50 of ∼2 Mb. Using comparative genomics tools, we explore genome evolution across available spider assemblies. Our findings suggest that the previously reported and vast genome size variation in spiders is linked to the different representation and number of transposable elements. Using statistical tools to uncover gene-family level evolution, we find expansions associated with the sensory perception of taste, immunity, and metabolism. In addition, we report strikingly different histories of chemosensory, venom, and silk gene families, with the first two evolving much earlier, affected by the ancestral whole genome duplication in Arachnopulmonata (∼450 Ma) and exhibiting higher numbers. Together, our findings reveal that spider genomes are highly variable and that genomic novelty may have been driven by the burst of an ancient whole genome duplication, followed by gene family and transposable element expansion.

Chromosome-Level Genome Assembly of the Common Chaffinch (Aves: Fringilla coelebs): A Valuable Resource for Evolutionary Biology.

The common chaffinch, Fringilla coelebs, is one of the most common, widespread, and well-studied passerines in Europe, with a broad distribution encompassing Western Europe and parts of Asia, North Africa, and the Macaronesian archipelagos. We present a high-quality genome assembly of the common chaffinch generated using Illumina shotgun sequencing in combination with Chicago and Hi-C libraries. The final genome is a 994.87-Mb chromosome-level assembly, with 98% of the sequence data located in chromosome scaffolds and a N50 statistic of 69.73 Mb. Our genome assembly shows high completeness, with a complete BUSCO score of 93.9% using the avian data set. Around 7.8% of the genome contains interspersed repetitive elements. The structural annotation yielded 17,703 genes, 86.5% of which have a functional annotation, including 7,827 complete universal single-copy orthologs out of 8,338 genes represented in the BUSCO avian data set. This new annotated genome assembly will be a valuable resource as a reference for comparative and population genomic analyses of passerine, avian, and vertebrate evolution.

A high-quality genome assembly and annotation of the gray mangrove, Avicennia marina.

The gray mangrove [Avicennia marina (Forsk.) Vierh.] is the most widely distributed mangrove species, ranging throughout the Indo-West Pacific. It presents remarkable levels of geographic variation both in phenotypic traits and habitat, often occupying extreme environments at the edges of its distribution. However, subspecific evolutionary relationships and adaptive mechanisms remain understudied, especially across populations of the West Indian Ocean. High-quality genomic resources accounting for such variability are also sparse. Here we report the first chromosome-level assembly of the genome of A. marina. We used a previously release draft assembly and proximity ligation libraries Chicago and Dovetail HiC for scaffolding, producing a 456,526,188-bp long genome. The largest 32 scaffolds (22.4-10.5 Mb) accounted for 98% of the genome assembly, with the remaining 2% distributed among much shorter 3,759 scaffolds (62.4-1 kb). We annotated 45,032 protein-coding genes using tissue-specific RNA-seq data in combination with de novo gene prediction, from which 34,442 were associated to GO terms. Genome assembly and annotated set of genes yield a 96.7% and 95.1% completeness score, respectively, when compared with the eudicots BUSCO dataset. Furthermore, an FST survey based on resequencing data successfully identified a set of candidate genes potentially involved in local adaptation and revealed patterns of adaptive variability correlating with a temperature gradient in Arabian mangrove populations. Our A. marina genomic assembly provides a highly valuable resource for genome evolution analysis, as well as for identifying functional genes involved in adaptive processes and speciation.