Molecular biology and evolution最新文献

Genome size varies widely, even among closely related species, yet much less is known about chromosome size variation. Here we use the fourth chromosome of Drosophila, also known as the "Muller F element" or "dot chromosome", as a model to investigate chromosome-specific size expansion. The F element of most Drosophila species is small (∼1.3 Mb) and almost entirely heterochromatic, yet harbors approximately 80 protein-coding genes. Here, we study D. kikkawai, D. takahashii, D. ananassae, and D. bipectinata, whose F elements are 2- to 15-fold larger in size compared to D. melanogaster. Through manual gene curation and comparative genomic analysis, we find that their F elements have expanded primarily via accumulation of transposable elements (TEs) in introns and intergenic regions. Natural selection appears less efficient on these expanded F elements: they have smaller effective population sizes and their genes exhibit reduced usage of optimal codons, compared to D. melanogaster. We propose that F element size variation is driven by differences in F element recombination rates. The ultra-long (∼20 Mb) F elements of D. ananassae and D. bipectinata display high rates of rearrangement and sequence evolution and exhibit independent TE-driven expansions. Our results suggest that F elements of most Drosophila species likely recombine enough to prevent size expansion, while F element recombination in D. ananassae and D. bipectinata is either absent or rare enough to allow TEs and other deleterious mutations to accumulate via Muller's ratchet; thus, these chromosomes evolve more like a Y chromosome than a typical Drosophila F element.

The testicular descent leading to the exteriorization of male gonads is a complex sexual dimorphic process observed in numerous mammals, whereas some species, such as elephants and cetaceans, retain the lifelong ascrotal testes. Despite the implication of Wnt signaling in testicular development and descent, the evolutionary mechanisms underlying ascrotal testes have not been adequately addressed. Here, we examined selection signatures and unique amino-acid substitutions in genes of the Wnt signaling pathway. We identified an ascrotal mammal-specific substitution (S406G) in ZNRF3 located within the DVL-interaction region. Functional assays showed that this substitution enhances the affinity of ascrotal ZNRF3 for DVLs and suppresses Wnt3a-induced Wnt signaling. Comparative transcriptomics of the gubernaculum between male fetal rats from wild-type and spontaneous cryptorchid (orl) strains revealed upregulation of Ctnnb1 and Gsk3b in orl rats, along with ascrotal-specific evolutionary changes in regulatory elements. Collectively, these findings suggest that Wnt signaling may be dampened in ascrotal mammals. This study provides insights into the pathogenesis of cryptorchidism in humans and domestic animals.

The testicular descent leading to the exteriorization of male gonads is a complex sexual dimorphic process observed in numerous mammals, whereas some species, such as elephants and cetaceans, retain the lifelong ascrotal testes. Despite the implication of Wnt signaling in testicular development and descent, the evolutionary mechanisms underlying ascrotal testes have not been adequately addressed. Here, we examined selection signatures and unique amino-acid substitutions in genes of the Wnt signaling pathway. We identified an ascrotal mammal-specific substitution (S406G) in ZNRF3 located within the DVL-interaction region. Functional assays showed that this substitution enhances the affinity of ascrotal ZNRF3 for DVLs and suppresses Wnt3a-induced Wnt signaling. Comparative transcriptomics of the gubernaculum between male fetal rats from wild-type and spontaneous cryptorchid (orl) strains revealed upregulation of Ctnnb1 and Gsk3b in orl rats, along with ascrotal-specific evolutionary changes in regulatory elements. Collectively, these findings suggest that Wnt signaling may be dampened in ascrotal mammals. This study provides insights into the pathogenesis of cryptorchidism in humans and domestic animals.

Metazoan oxidative phosphorylation (OXPHOS) complexes are composed of subunits encoded by mitochondrial and nuclear genes, requiring continuous mitonuclear coevolution to ensure functional compatibility. However, mitochondrial and nuclear genomes exhibit separate inheritance patterns, leading to their distinct or even conflicting evolutionary histories. This study aimed to analyse phylogenetic signals among mitochondrial genes, nuclear-encoded OXPHOS genes, and general nuclear genes across 53 beetle species. Two major cases of mitonuclear discordance were detected. The nuclear-encoded OXPHOS genes supported mitochondrial phylogenetic signals in noterids, indicating that in noterids the evolutionary history of OXPHOS complexes diverged from the phylogenetic history. Conversely, nuclear-encoded OXPHOS genes aligned with the phylogenetic history of rhysodines, and this mitonuclear discordance suggests that mitochondrial genomes exhibited clear signatures of genetic introgression. By integrating phylogenetic reconstructions and reticulate evolutionary network analyses, we attributed the mitonuclear discordance in noterids to incomplete lineage sorting. In contrast, the mitochondrial genomes of rhysodines underwent introgressive hybridization events. Although mitonuclear incompatibility is typically resolved by nuclear compensatory mechanisms, our findings indicate that nuclear compensation exhibits limited efficacy at the gene level, yet locally adaptive residues persist. This was further supported by the weak correlation between nuclear-encoded OXPHOS genes and mitochondrial genes, with no robust mitonuclear coevolutionary signals detected. These findings collectively suggest a loose mitonuclear interaction in beetles. The decoupling of mitochondrial and nuclear evolutionary trajectories may serve as an evolutionary "buffer" to accommodate genomic conflicts while maintaining essential OXPHOS systems.

Selection is a fundamental evolutionary force that shapes patterns of genetic variation across species. However, simulations incorporating realistic selection along heterogeneous genomes in complex demographic histories are challenging, limiting our ability to benchmark statistical methods aimed at detecting selection and to explore theoretical predictions. stdpopsim is a community-maintained simulation library that already provides an extensive catalog of species-specific population genetic models. Here, we present a major extension to the stdpopsim framework that enables simulation of various modes of selection, including background selection, selective sweeps, and arbitrary distributions of fitness effects (DFE) acting on annotated subsets of the genome (for instance, exons). This extension maintains stdpopsim's core principles of reproducibility and accessibility while adding support for species-specific genomic annotations and published DFE estimates. We demonstrate the utility of this framework by comparing methods for demographic inference, DFE estimation, and selective sweep detection across several species and scenarios. Our results demonstrate the robustness of demographic inference methods to selection on linked sites, reveal the sensitivity of DFE-inference methods to model assumptions, and show how genomic features, like recombination rate and functional sequence density, influence power to detect selective sweeps. This extension to stdpopsim provides a powerful new resource for the population genetics community to explore the interplay between selection and other evolutionary forces in a reproducible, user-friendly framework.

Mechanisms of X chromosome dosage compensation have been studied in model organisms with distinct sex chromosome ancestry. However, the diversity of mechanisms as a function of sex chromosome evolution is largely unknown. Here, we anchor ourselves to the nematode Caenorhabditis elegans, where dosage compensation is accomplished by an X chromosome-specific condensin that belongs to the family of structural maintenance of chromosomes (SMC) complexes. By combining a phylogenetic analyses of the C. elegans dosage compensation complex with a comparative analysis of its epigenetic signatures, such as X-specific topologically associating domains and enrichment of H4K20me1, we show that the condensin-mediated mechanism evolved recently in the lineage leading to Caenorhabditis following an SMC-4 duplication. Unexpectedly, we found an independent duplication of SMC-4 in Pristionchus pacificus along with X-specific topologically associating domains and H4K20me1 enrichment, which suggests that condensin-mediated dosage compensation evolved more than once in nematodes. Differential expression analysis between sexes in several nematode species indicates that dosage compensation itself precedes the evolution of X-specific condensins. In Rhabditina, X-specific condensins may have evolved in the presence of an existing mechanism linked to H4K20 methylation as Oscheius tipulae X chromosomes are enriched for H4K20me1 without SMC-4 duplication or topologically associating domains. In contrast, Steinernema hermaphroditum lacks H4K20me1 enrichment, SMC-4 duplication, and topologically associating domains. Together, our results indicate that dosage compensation mechanisms continue to evolve in species with shared X chromosome ancestry, and SMC complexes may have been co-opted at least twice in nematodes, suggesting that the process of evolving chromosome-wide gene regulatory mechanisms are constrained.

Trichomonas species are a diverse group of microbial eukaryotes (also commonly referred to as protists) that are obligate extracellular symbionts associated with or attributed to various inflammatory diseases. They colonize mucosal surfaces across a wide range of hosts, all of which harbor a resident microbiota. Their evolutionary history likely involved multiple host transfers, including zoonotic events from columbiform birds to mammals. Using comparative transcriptomics, this study examines Trichomonas gallinae co-cultured with Escherichia coli, identifying a molecular toolkit that Trichomonas species may use to interact with bacterial members of the microbiota. Integrating transcriptomic data with comparative genomics and phylogenetics revealed a conserved repertoire of protein-coding genes likely acquired through multiple lateral gene transfers (LGTs) in a columbiform-infecting ancestor. These LGT-derived genes encode muramidases, glucosaminidases, and antimicrobial peptides-enzymes and effectors capable of targeting bacterial cell walls, potentially affecting the bacterial-microbiota composition across both avian and mammalian hosts. This molecular toolkit suggests that Trichomonas species can actively compete with and exploit their surrounding microbiota for nutrients, potentially contributing to dysbiosis associated with Trichomonas infections. Their ability to target bacterial populations at mucosal surfaces provides insight into how Trichomonas species may have adapted to diverse hosts and how they could influence inflammatory mucosal diseases in birds and mammals.

Transposable elements (TEs) are abundant selfish genetic elements that can mobilize in their host genome, causing DNA damage, mutations, and chromosome rearrangements. TE silencing is thus critical, and is initiated by maternally loaded piRNAs, leading to their repression. Consistently, paternally inherited TEs are derepressed in the progeny of Drosophila crosses involving a naive female. TEs have also been found to be derepressed in interspecific crosses, which is proposed to result from suboptimal interactions of piRNA pathway proteins. Fundulus heteroclitus and F. diaphanus hybridize in nature and produce viable and fertile offspring that sometimes reproduce asexually. We characterized the repetitive DNA content of these species and their asexually reproducing hybrids. TE load was slightly higher than expected in hybrids and associated with younger repeats. Two biparentally inherited active Neptune subfamilies showed a remarkable ∼3- to 4-fold accumulation in hybrids. These results are consistent with suboptimal piRNA pathway function, leading to active TE accumulation.

Plasmids are important drivers of evolutionary transformations and ecological adaptation in prokaryotes. Plasmids supplying the host with beneficial functions may become domesticated and gain a stable inheritance within the host lineage. Domesticated plasmids may comprise core genes that are present in all taxon members. The origin of plasmid core genes remains poorly understood and alternative scenarios entailing gene translocation or genetic redundancy are debated. Studying plasmid evolution in the plant-associated Pantoea, we show that the large Pantoea plasmids (LPP-1 and LPP-2) are domesticated. We infer that the LPP-1 was acquired in the ancestor of plant-associated Pantoea species. The LPP-2 acquisition is traced to the ancestor of plant growth-promoting species. We show that both plasmids are vertically inherited and the LPP-1 replication is furthermore coordinated with chromosome replication. Both plasmids harbor core gene families at the genus (LPP-1) or species (LPP-2) level. Using phylogenomics we infer a deep divergence between plasmid and chromosomal core genes, indicating rare gene translocation between the replicons. Our results suggest that the LPP-1 and LPP-2 acquisition introduced genetic redundancy with chromosomal genes, that was followed by successive waves of differential gene loss. The domestication of both plasmids likely contributed to species divergence in Pantoea.

Mutator phenotypes are short-lived due to the rapid accumulation of deleterious mutations. Yet, recent observations reveal that certain fungi can undergo prolonged accelerated evolution after losing genes involved in DNA repair. Here, we surveyed 1,154 yeast genomes representing nearly all known yeast species of the subphylum Saccharomycotina (phylum Ascomycota) to examine the relationship between reduced gene repertoires broadly associated with genome stability functions (eg DNA repair, cell cycle) and elevated evolutionary rates. We identified 3 distantly related lineages-encompassing 12% of species-that had both the most streamlined sets of genes involved in genome stability (specifically DNA repair) and the highest evolutionary rates in the entire subphylum. Two of these "faster-evolving lineages" (FELs)-a subclade within the order Pichiales and the Wickerhamiella/Starmerella (W/S) clade (order Dipodascales)-are described here for the first time, while the third corresponds to a previously documented Hanseniaspora FEL. Examination of genome stability gene repertoires revealed a set of genes predominantly absent in these 3 FELs, suggesting a potential role in the observed acceleration of evolutionary rates. In the W/S clade, genomic signatures are consistent with a substantial mutational burden, including pronounced A|T bias and endogenous DNA damage. Interestingly, we found that the W/S clade also contains DNA repair genes possibly acquired through horizontal gene transfer, including a photolyase of bacterial origin. These findings highlight how hypermutators can persist across macroevolutionary timescales, potentially linked to the loss of genes related to genome stability, with horizontal gene transfer as a possible avenue for partial functional compensation.