Abstract Differentiating between genes that evolve under neutral drift versus stabilizing selection is one of the first explorations in comparative phylogenomic studies. Neutral drift and stabilizing selection of gene expression levels across a phylogeny are modelled using a Brownian motion and an Ornstein-Uhlenbeck process, respectively. Most empirical gene expression datasets contain only a few species, raising concerns about statistical power for model selection and parameter estimation. Furthermore, gene expression datasets often contain multiple samples per species, contrary to common macroevolutionary analyses of trait evolution. Here, we designed a targeted simulation study to evaluate the power to identify stabilizing selection, emphasizing the impact of the number of species, strength of selection and within-species variances. Our results show that the accuracy of selection strength estimation improves with increasing phylogeny size. Distinguishing weak selection, i.e., lower selection strength, from neutral drift is challenging, whereas varying levels of within-species variance have only minor effects on parameter estimation and model selection. Overall, our results suggest that we can have sufficient power to detect stabilizing selection with approximately 17 species, if the underlying strength of selection is sufficiently strong and if a relatively relaxed statistical significance threshold is adopted.
Abstract Small nucleolar RNAs (snoRNAs) are best known for guiding chemical modifications of ribosomal and spliceosomal RNAs. Most vertebrate snoRNAs are encoded within introns of host genes and therefore depend on the production and processing of host precursor RNAs for their biogenesis. Despite this close genomic association, how host-gene context is associated with snoRNA abundance and evolution remains poorly understood. Here, we combined human snoRNA annotations from snoDB, Ensembl gene annotations, snoRNA-sensitive abundance data across multiple tissues, and vertebrate orthology analyses to systematically characterize snoRNA–host-gene relationships. Host genes were grouped into functional classes to compare snoRNA genomic organization, abundance, and conservation across host contexts. We confirmed that snoRNAs are enriched in ribosome-related and lncRNA host genes. SnoRNAs embedded in ribosome-related host genes, particularly ribosomal protein genes, showed the highest abundance and were predominantly broadly detected across tissues, whereas snoRNAs in other host classes were generally less abundant and more tissue-restricted. Across vertebrates, snoRNA sequences were often widely conserved, but the exact host-gene association was less stable, showing that sequence conservation can persist despite changes in genomic embedding. Ribosome-related host classes nevertheless emerged as comparatively stable environments. Together, these results show that snoRNA–host-gene relationships vary across host contexts and evolutionary histories and are consistent with a conceptual continuum from functionally concordant associations to more independent passenger relationships.
Abstract Eurosta solidaginis is a plant-parasitic insect that develops from egg to adult inside of a spheroid gall it induces on the stem of goldenrod plants (Solidago spp.). E. solidaginis is widespread across North America, with a geographic distribution that extends from Southern Canada to Texas and the Southern U.S. and from the Atlantic coast to the Great Plains and includes scattered populations reaching the West coast. The natural history, ecology and physiology of E. solidaginis are well-documented, and its overwintering physiology, multitrophic interactions, and ecological speciation have been well-studied. Surprisingly, genomic resources are restricted to an incomplete scaffold-level genome assembly lacking protein-coding gene annotation. To advance understanding of the physiology, gall-forming, and population structure of E. solidaginis, we sequenced and assembled the genome of a single pupa using PacBio HiFi sequencing and Hi-C chromatin proximity sequencing technology. Here, we present a fully-annotated, chromosome-level de novo assembly of the 1.9 Gb genome, spanning five autosomes and the sex chromosomes. The assembly has a contig N50 of 3.7 Mb and a scaffold N50 of 289.3 Mb, and 96.5% of expected Diptera BUSCOs in the genome found in single copy. We annotated 14,223 identified protein-coding genes, identifying 96.2% of BUSCOs in the protein set found in single copy. The 18,293 bp mitochondrial genome was assembled and subsequently annotated separately. Even though there are 400-450 gall-inducing tephritid species, this is the second high-quality, chromosome-level genome assembly of a gall-forming fly in the family, and the third freeze tolerant dipteran genome.
Abstract Patagonia represents the final frontier of the human out-of-Africa expansion, where humans have lived for at least 13,500 years, yet the genetic adaptations of its indigenous populations remain understudied. We analyzed genome-wide data from 71 present-day individuals across 7 Patagonian locations. Our analyses reveal widespread European admixture initiating approximately 10 to 12 generations ago, followed by region-specific demographic trajectories. We identified a profound north-south genetic differentiation. Populations from the Chiloé Archipelago and Argentinean Patagonia share ancestry with the Mapuche, whereas individuals from Tierra del Fuego exhibit a unique, deeply rooted genetic component shared with ancient Fueguian groups. To identify prehistoric local adaptations, we performed selection scans on masked Native American genomic segments. We detected robust selection signals predating European contact in genes associated with height and skeletal development (SUPT3H, CADM1, RUNX2), lipid metabolism (MSMO1, LYPLA1, SORT1/PSCR1/CELSR2), and energy homeostasis (ZNF202). Furthermore, we observed a significant enrichment of Native American ancestry within the Major Histocompatibility Complex on chromosome 6. In conclusion, our findings indicate that the current admixed populations in Patagonia exhibit signals of local adaptation that likely originated in their ancient indigenous ancestors. These groups accumulated critical morphological, metabolic, and immunological adaptations to their extreme environment and local pathogens, traits that remained highly beneficial even after European admixture.
Abstract The immune system plays key roles in the mammalian uterine cycle, particularly for menstruation, a dramatic tissue renewal mechanism independently acquired four times in eutherians. These roles specifically involve NK cells through the expression of surface killer cell immunoglobulin-like receptors (KIRs) and killer cell lectin-like receptors (KLRs), respectively part of the immunoglobulin-like and lectin-like gene superfamilies with poorly resolved phylogenetic histories. Acquisition of menstruation in primates seemingly coincides with a large expansion of the KIR family, suggesting that innovations in NK cell receptor families may have been crucial for the evolution of menstruation. To test this hypothesis, we performed an in-depth analysis of the evolutionary histories of the KIR and KLR gene families across 41 mammalian genomes, including all four clades that acquired menstruation. Our results reveal the existence of undescribed KIR and KLR genes across many mammalian species, including elephants, armadillos, rhinoceroses, and leaf-nosed bats, as well as a novel subfamily within the KLR phylogeny. Altogether, we identify more than twice as many NK cell receptor genes across mammals than currently reported in reference genomes. Further, we show that the KIR gene family has experienced intensified purifying selection in menstruating species compared to non-menstruating species, suggesting specific evolutionary pressures related to menstruation and illustrating gene-level convergence linked to the phenotype. Our data, however, do not support that menstruation coincides with expansions or contractions in NK cell receptor repertoires, except in primates, highlighting both shared and lineage-specific immune adaptations to rapidly evolving reproductive biology.
