Genome Biology and Evolution最新文献

Subsociality and wood-eating or xylophagy are understood as key drivers in the evolution of eusociality in Blattodea (cockroaches and termites), two features observed in the cockroach genus Cryptocercus, the sister group of all termites. We analyse two high-quality genomes from this genus, C. punctulatus from North America and C. meridianus from Southeast Asia, to explore the evolutionary transitions to xylophagy and subsociality within Blattodea. Our analyses reveal evidence of relaxed selection in both Cryptocercus and termites, indicating that a reduction in effective population size may have occurred in their subsocial ancestors. These findings challenge the expected positive correlation between dN/dS ratios and social complexity, as Cryptocercus exhibits elevated dN/dS values that may exceed those of eusocial termites. Additionally, we infer a reduction in the number of Ionotropic Receptors and a change from uni- to bimodal methylation signatures in protein coding genes in a common ancestor of Cryptocercus and termites, mechanisms previously thought to have evolved with the emergence of eusociality in termites. Future studies incorporating additional genomic data from diverse blattodean species can further build on these findings and provide deeper insights into the molecular mechanisms driving transitions to xylophagy and eusociality.

Germline mutation rates are fundamental to evolution, yet they remain unquantified for beetles (Coleoptera), the most speciose order including major pests. We sequenced genomes from 16 trios of the Colorado potato beetle (Leptinotarsa decemlineata, CPB)-a pest evolved resistance to many insecticides. We estimated a germline mutation rate of 5.8 × 10-9 (95%CI: 4.7 × 10-9, 7.2 × 10-9) per site per generation in CPB, a rate 2-fold higher than the median for other insects. Across 13 insect species, mutation rate was positively associated with genome-wide GC content (PGLS). The increased mutation rates in CPB is also consistent with drift-barrier expectations. Based on this mutation rate and the beetle's fecundity, we estimate that the brood from just one CPB female can introduce nearly 141 new mutations into the coding regions each generation. These findings inform CPB's rapid pesticide resistance evolution and fill a key gap in arthropod genomics and evolution.

Sex chromosome evolution and gene regulation are closely linked but remain understudied in many taxa. Young neo-sex chromosomes offer unique insights into these processes. We examine dosage compensation (DC) and sex-biased gene expression in Vandiemenella viatica grasshoppers by comparing the ancestral X chromosome in the P24X0 race with derived neo-sex chromosomes in the P24XY race. The P24XY neo-XY arose via X-autosome fusion: the XL arm represents the ancestral X and the XR arm a former autosome (chromosome 1 in P24X0) now part of the neo-X and homologous to the neo-Y. We first assess DC via male and female gene expression. In somatic tissues, male P24X0 X-linked and P24XY XL-linked genes are upregulated to match both female expression and autosomal levels, indicating near-complete DC. In testes, expression of X-linked and the XL-linked genes is reduced nearly fourfold reflecting absent DC and the presence of meiotic X chromosome inactivation. We then analyse sex-biased gene expression across tissues and chromosomes. Gonads show stronger sex-biased gene expression than somatic tissues. Female-biased genes are concentrated on the P24X0 X and P24XY XL, where male-biased genes are enriched on autosomes and the XR arm of the neo-X. Overall, the ancestral X in P24X0 and the XL arm of the P24XY neo-X are hypertranscribed, while the XR arm retains autosomal expression, male-biased enrichment, and lacks DC. These patterns show that DC is regulated at levels of chromosome arms and illustrate how chromosome structure, gene regulation, and reproduction interact, shedding light on sex chromosome evolution in V. viatica.

Viral domestication, the co-option of integrated viral genes for host functions, has been repeatedly documented in endoparasitoid Hymenoptera. Whether this phenomenon extends to other parasitoid insects remains to be assessed. Here, we tested this hypothesis in tachinid flies, the largest group of non-hymenopteran parasitoids. To this end, we investigated patterns of viral endogenization in 52 genomes, including 37 newly sequenced species. Similarly to hymenopteran endoparasitoids, tachinid genomes were found to display numerous endogenous viral elements (EVEs), primarily derived from insect-infecting viruses with either DNA or RNA genomes. However, the majority of integrated sequences were species-specific, with no evidence of major ancient gene domestication events. In addition, the EVE content did not differ between dipteran parasitoids and their free-living Diptera counterparts. These findings contrast with the recurrent viral domestication observed in endoparasitoid Hymenoptera. This pattern is discussed in light of important attributes of tachinid flies including their lack of venom and perforating ovipositor, and their avoidance of the host immune system.

Mitochondrial genomes offer valuable insights into biological and phylogenetic processes, yet the factors shaping their architecture across metazoan lineages remain poorly understood, largely due to limited taxonomic sampling. To address this gap, we analyzed mitochondrial genomes from 20 species spanning a broad taxonomic spectrum of the phylum Gastrotricha. Our findings, supported by phylogenetic analyses based on mitochondrial datasets, reveal two distinct evolutionary patterns: one lineage displays remarkable conservation in genome structure, while the other exhibits variability in gene content, arrangement, strand polarity, and repeat abundance. These contrasting patterns appear to be related to differences in reproductive strategies (hermaphroditism vs. parthenogenesis) and ecological habitats (marine vs. freshwater). While these associations are intriguing, further data are needed to understand the underlying processes. This study highlights the importance of broad phylum-scale mitogenomic sampling for uncovering genomic diversity and advancing our understanding of mitochondrial evolution across Metazoa.

Chromosomal rearrangements, particularly those mediated by transposable elements (TEs), can drive adaptive evolution by creating chimeric genes, inducing de novo gene formation, or altering gene expression. Here, we investigate rearrangements evolutionary role during habitat shifts in two locally adapted populations, D. santomea and D. yakuba, who have inhabited the island São Tomè for 500,000 and 10,000 years, respectively. Using the D. yakuba-D. santomea species complex, we identified 16,480 rearrangements in the two island populations and the ancestral mainland African population of D. yakuba. We find a disproportionate association with TEs, with 83.5% of rearrangements linked to TE insertions or TE-facilitated ectopic recombination. Using significance thresholds based on neutral expectations, we identify 383 and 468 significantly differentiated rearrangements in island D. yakuba and D. santomea, respectively, relative to the mainland population. Of these, 99 and 145 rearrangements also showed significant differential gene expression, highlighting the potential for adaptive solutions from rearrangements and TEs. Within and between island populations, we find significantly different proportions of rearrangements originating from new mutations versus standing variation depending on TE association, potentially suggesting adaptive genetic mechanisms differ based on the timing of habitat shifts. Functional analyses of rearrangements most likely driving local adaptation revealed enrichment for stress response pathways, including UV tolerance and DNA repair, in high-altitude D. santomea. These findings suggest that chromosomal rearrangements may act as a source of genetic innovation, and provides insight into evolutionary processes that SNP-based analyses might overlook.

Biodiversity conservation relies upon accurate species taxonomy to support decision-making. Stony corals in the genus Pocillopora are critical ecosystem engineers in the Eastern Tropical Pacific (ETP); however, Pocillopora species diversity in the region is still unresolved due to high phenotypic plasticity, lack of diagnostic morphological characters, and low-resolution genetic markers used in previous studies. To address this gap, we leveraged low-coverage whole-genome sequencing for 342 Pocillopora coral samples collected from Panamá, Costa Rica, Colombia, Ecuador, and Clipperton Atoll (France). Sequence data were used to recover mitochondrial genomes and barcode loci, ultraconserved elements, and genome-wide single-nucleotide polymorphisms (SNPs) for species delimitation. Together, our data revealed the existence of four distinct Pocillopora species in the ETP, corresponding to the nominal species P. effusa (Veron, 2000), P. meandrina Dana, 1846, P. capitata Verrill, 1864, and P. lacera Verrill, 1869. Two P. capitata population subclusters with moderate genetic differentiation were separated between offshore islands and continental sites, and individual colonies with signatures of admixture between P. effusa and P. lacera were identified at Isla del Coco, Costa Rica. Additionally, Pocillopora-associated algal symbiont community profiling identified Cladocopium and Durusdinium as dominant genera that varied according to the host species, with P. lacera demonstrating higher specificity for associations with Cladocopium. This study highlights the power of genome skimming as an affordable, high-resolution approach to rapidly assess coral species diversity and algal symbiont associations, thereby empowering marine conservation.

Domestication of transposable elements has been extensively documented in vertebrates, but few examples have been reported in nonmodel organisms, particularly crustaceans. Here, we present Imagin (Integrase-like gene in MAlacostracans derived from GINger1), a gene family derived from a Ginger1 DNA transposon domesticated in the common ancestor of malacostracan crustaceans over 400 million years ago. We discovered Imagin in the kuruma shrimp Penaeus japonicus as a single-copy, multiexon gene residing within a conserved intron of the methylmalonyl-CoA mutase (MMUT) gene. Comprehensive phylogenetic and structural analyses demonstrate that while Imagin orthologs are under strong purifying selection and retain the conserved H2C2 zinc-finger domain and integrase core, they have ubiquitously lost the catalytic DDE triad essential for endonuclease activity. These structural features indicate that Imagin has undergone molecular exaptation, abandoning its ancestral mobility for a host function. Consistent with this loss of enzymatic capacity, PjImagin protein accumulates predominantly in the cytosol of oocytes during early development, rather than the nucleus. This localization pattern implies that the gene has been co-opted for a noncatalytic role, potentially involving nucleic acid binding, during female gonadal development in penaeid shrimp. Furthermore, transcriptome data revealed divergent expression profiles across lineages, where Imagin is enriched in the ovaries of penaeid shrimp but predominantly in the testes of other decapods, such as crabs and lobsters. Imagin thus represents a novel case of TE evolution, illustrating a complex history of ancient domestication followed by structural remodeling and regulatory subfunctionalization.

Understanding how extant physiological landscapes arise from novel genetic interactions is key to elucidating phenotypic evolution. Sperm cells exemplify a striking case of functional compartmentalization shaped by molecular adjustments, notably regarding energy metabolism. Here, we examine the impact of gene duplication and loss on the evolution of sperm energetics in mammals. Our findings reveal that the acquisition of an exclusive mechanism controlling the sperm plasma membrane Na+ gradient, critical for glucose uptake, emerged in the ancestor of mammals through gene duplication, which originated the Na+/K+ ATPase transporting subunit alpha 4 transporter (Atp1a4). Furthermore, we demonstrate that testis-specific expression of Atp1a4 was acquired after the divergence from monotremes. Notably, we identify three independent pseudogenization events of Atp1a4, including in pangolins, the naked mole-rat (Heterocephalus glaber) and toothed whales. The recurrent loss of function in Atp1a4 coincides with the erosion of the testis-specific glycolytic pathway in these lineages. Furthermore, enrichment analysis of striped dolphin (Stenella coeruleoalba) and naked mole-rat testis transcriptomes also suggests significant alterations in sperm capacitation processes. Overall, we show that the elaboration of a sodium-dependent glucose uptake wiring was a key innovation in the energetic landscape governing mammalian spermatozoa, with secondary gene loss in three separate lineages pointing to drastic alterations in motility and capacitation processes. Our findings illustrate how metabolic pathways co-shaped by gene duplication and erosion define extant physiological phenotypes.

Large surface proteins in bacteria serve important functions in aggregation, biofilm formation, and cell interaction processes. In Apilactobacillus kunkeei, a defensive symbiont of the honeybee Apis mellifera, as much as 6% of the 1.5 Mb genome consists of 5 consecutive genes for extracellular surface proteins of 3,000 to 8,000 amino acids, named Giant1-5. Here, we predict the structures of these proteins and provide a study of their origin and evolution. The structure predictions suggest that the Giant1-4 proteins contain a β-solenoid domain at their N-terminal ends with similarity to the β-solenoid domain in serine-rich repeat proteins, which mediates binding to glycoproteins, polysaccharides, and epithelial cells. Phylogenetic analyses based on the β-solenoid domains of the Giant1-3 proteins indicate sequence exchange between 2 genera of otherwise distantly related obligate fructophilic lactic acid bacteria, while the diversification of the positional homologs of the giant1-3 genes in the A. kunkeei population is mostly due to short, intra-genic recombination events. Genes for the Giant4-5 proteins were only identified in A. kunkeei and 2 closely related bacterial species, suggesting that they were added to the giant gene cluster more recently. The phylogenetic analyses indicate co-evolution of the giant4-5 genes in A. kunkeei, and the near sequence identity of one of the 2 giant4-5 subtypes correlates with predicted recombination events that span across both genes. Our findings provide new insights into the evolution of very large surface proteins in the bacterial ecosystem adapted to the carbohydrate-rich growth niches provided by bees, their food sources, and food products.