Increased Positive Selection in Highly Recombining Genes Does not Necessarily Reflect an Evolutionary Advantage of Recombination.

It is commonly thought that the long-term advantage of meiotic recombination is to dissipate genetic linkage, allowing natural selection to act independently on different loci. It is thus theoretically expected that genes with higher recombination rates evolve under more effective selection. On the other hand, recombination is often associated with GC-biased gene conversion (gBGC), which theoretically interferes with selection by promoting the fixation of deleterious GC alleles. To test these predictions, several studies assessed whether selection was more effective in highly recombining genes (due to dissipation of genetic linkage) or less effective (due to gBGC), assuming a fixed distribution of fitness effects (DFE) for all genes. In this study, I directly derive the DFE from a gene's evolutionary history (shaped by mutation, selection, drift, and gBGC) under empirical fitness landscapes. I show that genes that have experienced high levels of gBGC are less fit and thus have more opportunities for beneficial mutations. Only a small decrease in the genome-wide intensity of gBGC leads to the fixation of these beneficial mutations, particularly in highly recombining genes. This results in increased positive selection in highly recombining genes that is not caused by more effective selection. Additionally, I show that the death of a recombination hotspot can lead to a higher dN/dS than its birth, but with substitution patterns biased towards AT, and only at selected positions. This shows that controlling for a substitution bias towards GC is therefore not sufficient to rule out the contribution of gBGC to signatures of accelerated evolution. Finally, although gBGC does not affect the fixation probability of GC-conservative mutations, I show that by altering the DFE, gBGC can also significantly affect nonsynonymous GC-conservative substitution patterns.

Structural variant landscapes reveal convergent signatures of evolution in sheep and goats.

BACKGROUND: Sheep and goats have undergone domestication and improvement to produce similar phenotypes, which have been greatly impacted by structural variants (SVs). Here, we report a high-quality chromosome-level reference genome of Asiatic mouflon, and implement a comprehensive analysis of SVs in 897 genomes of worldwide wild and domestic populations of sheep and goats to reveal genetic signatures underlying convergent evolution. RESULTS: We characterize the SV landscapes in terms of genetic diversity, chromosomal distribution and their links with genes, QTLs and transposable elements, and examine their impacts on regulatory elements. We identify several novel SVs and annotate corresponding genes (e.g., BMPR1B, BMPR2, RALYL, COL21A1, and LRP1B) associated with important production traits such as fertility, meat and milk production, and wool/hair fineness. We detect signatures of selection involving the parallel evolution of orthologous SV-associated genes during domestication, local environmental adaptation, and improvement. In particular, we find that fecundity traits experienced convergent selection targeting the gene BMPR1B, with the DEL00067921 deletion explaining ~10.4% of the phenotypic variation observed in goats. CONCLUSIONS: Our results provide new insights into the convergent evolution of SVs and serve as a rich resource for the future improvement of sheep, goats, and related livestock.

Effect of locomotor preference on the evolution of mitochondrial genes in Bovidae.

Locomotor preferences and habitat types may drive animal evolution. In this study, we speculated that locomotor preference and habitat type may have diverse influences on Bovidae mitochondrial genes. We used selection pressure and statistical analysis to explore the evolution of mitochondrial DNA (mtDNA) protein-coding genes (PCGs) from diverse locomotor preferences and habitat types. Our study demonstrates that locomotor preference (energy demand) drives the evolution of Bovidae in mtDNA PCGs. The habitat types had no significant effect on the rate of evolution in Bovidae mitochondrial genes. Our study provides deep insight into the adaptation of Bovidae.

Evolutionary radiation strategy revealed in the Scarabaeidae with evidence of continuous spatiotemporal morphology and phylogenesis.

Evolutionary biology faces the important challenge of determining how to interpret the relationship between selection pressures and evolutionary radiation. The lack of morphological evidence on cross-species research adds to difficulty of this challenge. We proposed a new paradigm for evaluating the evolution of branches through changes in characters on continuous spatiotemporal scales, for better interpreting the impact of biotic/abiotic drivers on the evolutionary radiation. It reveals a causal link between morphological changes and selective pressures: consistent deformation signals for all tested characters on timeline, which provided strong support for the evolutionary hypothesis of relationship between scarabs and biotic/abiotic drivers; the evolutionary strategies under niche differentiation, which were manifested in the responsiveness degree of functional morphological characters with different selection pressure. This morphological information-driven integrative approach sheds light on the mechanism of macroevolution under different selection pressures and is applicable to more biodiversity research.

Whole-genome sequencing reveals genomic diversity and selection signatures in Xia'nan cattle.

BACKGROUND: The crossbreeding of specialized beef cattle breeds with Chinese indigenous cattle is a common method of genetic improvement. Xia'nan cattle, a crossbreed of Charolais and Nanyang cattle, is China's first specialized beef cattle breed with independent intellectual property rights. After more than two decades of selective breeding, Xia'nan cattle exhibit a robust physique, good environmental adaptability, good tolerance to coarse feed, and high meat production rates. This study analyzed the population genetic structure, genetic diversity, and genomic variations of Xia'nan cattle using whole-genome sequencing data from 30 Xia'nan cattle and 178 published cattle genomic data. RESULT: The ancestry estimating composition analysis showed that the ancestry proportions for Xia'nan cattle were mainly Charolais with a small amount of Nanyang cattle. Through the genetic diversity studies (nucleotide diversity and linkage disequilibrium decay), we found that the genomic diversity of Xia'nan cattle is higher than that of specialized beef cattle breeds in Europe but lower than that of Chinese native cattle. Then, we used four methods to detect genome candidate regions influencing the excellent traits of Xia'nan cattle. Among the detected results, 42 genes (θπ and CLR) and 131 genes (FST and XP-EHH) were detected by two different detection strategies. In addition, we found a region in BTA8 with strong selection signals. Finally, we conducted functional annotation on the detected genes and found that these genes may influence body development (NR6A1), meat quality traits (MCCC1), growth traits (WSCD1, TMEM68, MFN1, NCKAP5), and immunity (IL11RA, CNTFR, CCL27, SLAMF1, SLAMF7, NAA35, and GOLM1). CONCLUSION: We elucidated the genomic features and population structure of Xia'nan cattle and detected some selection signals in genomic regions potentially associated with crucial economic traits in Xia'nan cattle. This research provided a basis for further breeding improvements in Xia'nan cattle and served as a reference for genetic enhancements in other crossbreed cattle.

Genome-wide analysis reveals genomic diversity and signatures of selection in Qinchuan beef cattle.

BACKGROUND: Indigenous Chinese cattle have abundant genetic diversity and a long history of artificial selection, giving local breeds advantages in adaptability, forage tolerance and resistance. The detection of selective sweeps and comparative genome analysis of selected breeds and ancestral populations provide a basis for understanding differences among breeds and for the identification and utilization of candidate genes. We investigated genetic diversity, population structure, and signatures of selection using genome-wide sequencing data for a new breed of Qinchuan cattle (QNC, n = 21), ancestral Qinchuan cattle (QCC, n = 20), and Zaosheng cattle (ZSC, n = 19). RESULTS: A population structure analysis showed that the ancestry components of QNC and ZSC were similar. In addition, the QNC and ZSC groups showed higher proportions of European taurine ancestry than that of QCC, and this may explain the larger body size of QNC, approaching that of European cattle under long-term domestication and selection. A neighbor-joining tree revealed that QCC individuals were closely related, whereas QNC formed a distinct group. To search for signatures of selection in the QNC genome, we evaluated nucleotide diversity (θπ), the fixation index (FST) and Tajima's D. Overlapping selective sweeps were enriched for one KEGG pathway, the apelin signaling pathway, and included five candidate genes (MEF2A, SMAD2, CAMK4, RPS6, and PIK3CG). We performed a comprehensive review of genomic variants in QNC, QCC, and ZSC using whole-genome sequencing data. QCC was rich in novel genetic diversity, while diversity in QNC and ZSC cattle was reduced due to strong artificial selection, with divergence from the original cattle. CONCLUSIONS: We identified candidate genes associated with production traits. These results support the success of selective breeding and can guide further breeding and resource conservation of Qinchuan cattle.

Strength of selection in lung tumors correlates with clinical features better than tumor mutation burden.

Single nucleotide substitutions are the most common type of somatic mutations in cancer genome. The goal of this study was to use publicly available somatic mutation data to quantify negative and positive selection in individual lung tumors and test how strength of directional and absolute selection is associated with clinical features. The analysis found a significant variation in strength of selection (both negative and positive) among tumors, with median selection tending to be negative even though tumors with strong positive selection also exist. Strength of selection estimated as the density of missense mutations relative to the density of silent mutations showed only a weak correlation with tumor mutation burden. In the "all histology together" analysis we found that absolute strength of selection was strongly correlated with all clinically relevant features analyzed. In histology-stratified analysis selection was strongest in small cell lung cancer. Selection in adenocarcinoma was somewhat higher compared to squamous cell carcinoma. The study suggests that somatic mutation- based quantifying of directional and absolute selection in individual tumors can be a useful biomarker of tumor aggressiveness.

A genomic hotspot of diversifying selection and structural change in the hoary bat (Lasiurus cinereus).

Background: Previous work found that numerous genes positively selected within the hoary bat (Lasiurus cinereus) lineage are physically clustered in regions of conserved synteny. Here I further validate and expand on those finding utilizing an updated L. cinereus genome assembly and additional bat species as well as other tetrapod outgroups. Methods: A chromosome-level assembly was generated by chromatin-contact mapping and made available by DNAZoo (www.dnazoo.org). The genomic organization of orthologous genes was extracted from annotation data for multiple additional bat species as well as other tetrapod clades for which chromosome-level assemblies were available from the National Center for Biotechnology Information (NCBI). Tests of branch-specific positive selection were performed for L. cinereus using PAML as well as with the HyPhy package for comparison. Results: Twelve genes exhibiting significant diversifying selection in the L. cinereus lineage were clustered within a 12-Mb genomic window; one of these (Trpc4) also exhibited diversifying selection in bats generally. Ten of the 12 genes are landmarks of two distinct blocks of ancient synteny that are not linked in other tetrapod clades. Bats are further distinguished by frequent structural rearrangements within these synteny blocks, which are rarely observed in other Tetrapoda. Patterns of gene order and orientation among bat taxa are incompatible with phylogeny as presently understood, implying parallel evolution or subsequent reversals. Inferences of positive selection were found to be robust to alternative phylogenetic topologies as well as a strong shift in background nucleotide composition in some taxa. Discussion: This study confirms and further localizes a genomic hotspot of protein-coding divergence in the hoary bat, one that also exhibits an increased tempo of structural change in bats compared with other mammals. Most genes in the two synteny blocks have elevated expression in brain tissue in humans and model organisms, and genetic studies implicate the selected genes in cranial and neurological development, among other functions.

Diversity of major histocompatibility complex of II B gene and mate choice in a monogamous and long-lived seabird, the Little Auk (Alle alle).

The major histocompatibility complex (MHC) plays a key role in the adaptive immune system of vertebrates, and is known to influence mate choice in many species. In birds, the MHC has been extensively examined but mainly in galliforms and passerines while other taxa that represent specific ecological and evolutionary life-histories, like seabirds, are underexamined. Here, we characterized diversity of MHC Class II B exon 2 in a colonial pelagic seabird, the Little Auk (or Dovekie Alle alle). We further examined whether MHC variation could be maintained through balancing selection and disassortative mating. We found high polymorphism at the genotyped MHC fragment, characterizing 99 distinct alleles across 140 individuals from three populations. The alleles frequencies exhibited a similar skewed distribution in both sexes, with the four most commonly occurring alleles representing approximately 35% of allelic variation. The results of a Bayesian site-by-site selection analysis suggest evidence of balancing selection and no direct evidence for MHC-dependent disassortative mating preferences in the Little Auk. The latter result might be attributed to the high overall polymorphism of the examined fragment, which itself may be maintained by the large population size of the species.

High heteroplasmy is associated with low mitochondrial copy number and selection against non-synonymous mutations in the snail Cepaea nemoralis.

Molluscan mitochondrial genomes are unusual because they show wide variation in size, radical genome rearrangements and frequently show high variation (> 10%) within species. As progress in understanding this variation has been limited, we used whole genome sequencing of a six-generation matriline of the terrestrial snail Cepaea nemoralis, as well as whole genome sequences from wild-collected C. nemoralis, the sister species C. hortensis, and multiple other snail species to explore the origins of mitochondrial DNA (mtDNA) variation. The main finding is that a high rate of SNP heteroplasmy in somatic tissue was negatively correlated with mtDNA copy number in both Cepaea species. In individuals with under ten mtDNA copies per nuclear genome, more than 10% of all positions were heteroplasmic, with evidence for transmission of this heteroplasmy through the germline. Further analyses showed evidence for purifying selection acting on non-synonymous mutations, even at low frequency of the rare allele, especially in cytochrome oxidase subunit 1 and cytochrome b. The mtDNA of some individuals of Cepaea nemoralis contained a length heteroplasmy, including up to 12 direct repeat copies of tRNA-Val, with 24 copies in another snail, Candidula rugosiuscula, and repeats of tRNA-Thr in C. hortensis. These repeats likely arise due to error prone replication but are not correlated with mitochondrial copy number in C. nemoralis. Overall, the findings provide key insights into mechanisms of replication, mutation and evolution in molluscan mtDNA, and so will inform wider studies on the biology and evolution of mtDNA across animal phyla.

The systematic codon usage bias has an important effect on genetic adaption in native species.

Random mutations increase genetic variety and natural selection enhances adaption over generations. Codon usage biases (CUB) provide clues about the genome adaptation mechanisms of native species and extremophile species. Significant numbers of gene (CDS) of nine classes of endangered, native species, including extremophiles and mesophiles were utilised to compute CUB. Codon usage patterns differ among the lineages of endangered and extremophiles with native species. Polymorphic usage of nucleotides with codon burial suggests parallelism of native species within relatively confined taxonomic groups. Utilizing the deviation pattern of CUB of endangered and native species, I present a calculation parameter to estimate the extinction risk of endangered species. Species diversity and extinction risk are both positively associated with the propensity of random mutation in CDS (Coding DNA sequence). Codon bias tenet profoundly selected and it governs to adaptive evolution of native species.

Terminal regions of a protein are a hotspot for low complexity regions and selection.

Volatile low complexity regions (LCRs) are a novel source of adaptive variation, functional diversification and evolutionary novelty. An interplay of selection and mutation governs the composition and length of low complexity regions. High %GC and mutations provide length variability because of mechanisms like replication slippage. Owing to the complex dynamics between selection and mutation, we need a better understanding of their coexistence. Our findings underscore that positively selected sites (PSS) and low complexity regions prefer the terminal regions of genes, co-occurring in most Tetrapoda clades. We observed that positively selected sites within a gene have position-specific roles. Central-positively selected site genes primarily participate in defence responses, whereas terminal-positively selected site genes exhibit non-specific functions. Low complexity region-containing genes in the Tetrapoda clade exhibit a significantly higher %GC and lower ω (dN/dS: non-synonymous substitution rate/synonymous substitution rate) compared with genes without low complexity regions. This lower ω implies that despite providing rapid functional diversity, low complexity region-containing genes are subjected to intense purifying selection. Furthermore, we observe that low complexity regions consistently display ubiquitous prevalence at lower purity levels, but exhibit a preference for specific positions within a gene as the purity of the low complexity region stretch increases, implying a composition-dependent evolutionary role. Our findings collectively contribute to the understanding of how genetic diversity and adaptation are shaped by the interplay of selection and low complexity regions in the Tetrapoda clade.

Molecular Evolution of Protein Sequences and Codon Usage in Monkeypox Viruses.

The monkeypox virus (mpox virus, MPXV) epidemic in 2022 has posed a significant public health risk. Yet, the evolutionary principles of MPXV remain largely unknown. Here, we examined the evolutionary patterns of protein sequences and codon usage in MPXV. We first demonstrated the signal of positive selection in OPG027, specifically in the Clade I lineage of MPXV. Subsequently, we discovered accelerated protein sequence evolution over time in the variants responsible for the 2022 outbreak. Furthermore, we showed strong epistasis between amino acid substitutions located in different genes. The codon adaptation index (CAI) analysis revealed that MPXV genes tended to use more non-preferred codons compared to human genes, and the CAI decreased over time and diverged between clades, with Clade I > IIa and IIb-A > IIb-B. While the decrease in fatality rate among the three groups aligned with the CAI pattern, it remains unclear whether this correlation was coincidental or if the deoptimization of codon usage in MPXV led to a reduction in fatality rates. This study sheds new light on the mechanisms that govern the evolution of MPXV in human populations.

Selection on the joint actions of pairs leads to divergent adaptation and coadaptation of care-giving parents during pre-hatching care.

The joint actions of animals in partnerships or social groups evolve under both natural selection from the wider environment and social selection imposed by other members of the pair or group. We used experimental evolution to investigate how jointly expressed actions evolve upon exposure to a new environmental challenge. Our work focused on the evolution of carrion nest preparation by pairs of burying beetles Nicrophorus vespilloides, a joint activity undertaken by the pair but typically led by the male. In previous work, we found that carrion nest preparation evolved to be faster in experimental populations without post-hatching care (No Care: NC lines) than with post-hatching care (Full Care: FC lines). Here, we investigate how this joint activity evolved. After 15 generations of experimental evolution, we created heterotypic pairs (NC females with FC males and NC males with FC females) and compared their carrion nest making with homotypic NC and FC pairs. We found that pairs with NC males prepared the nest more rapidly than pairs with FC males, regardless of the female's line of origin. We discuss how social coadaptations within pairs or groups could act as a post-mating barrier to gene flow.

Role-reversed polyandry is associated with faster fast-Z in shorebirds.

In birds, males are homogametic and carry two copies of the Z chromosome ('ZZ'), while females are heterogametic and exhibit a 'ZW' genotype. The Z chromosome evolves at a faster rate than similarly sized autosomes, a phenomenon termed 'fast-Z evolution'. This is thought to be caused by two independent processes-greater Z chromosome genetic drift owing to a reduced effective population size, and stronger Z chromosome positive selection owing to the exposure of partially recessive alleles to selection. Here, we investigate the relative contributions of these processes by considering the effect of role-reversed polyandry on fast-Z in shorebirds, a paraphyletic group of wading birds that exhibit unusually diverse mating systems. We find stronger fast-Z effects under role-reversed polyandry, which is consistent with particularly strong selection on polyandrous females driving the fixation of recessive beneficial alleles. This result contrasts with previous research in birds, which has tended to implicate a primary role of genetic drift in driving fast-Z variation. We suggest that this discrepancy can be interpreted in two ways-stronger sexual selection acting on polyandrous females overwhelms an otherwise central role of genetic drift, and/or sexual antagonism is also contributing significantly to fast-Z and is exacerbated in sexually dimorphic species.

Gene loss and relaxed selection of plaat1 in vertebrates adapted to low-light environments.

Gene loss is an important mechanism for evolution in low-light or cave environments where visual adaptations often involve a reduction or loss of eyesight. The plaat gene family encodes phospholipases essential for the degradation of organelles in the lens of the eye. These phospholipases translocate to damaged organelle membranes, inducing them to rupture. This rupture is required for lens transparency and is essential for developing a functioning eye. Plaat3 is thought to be responsible for this role in mammals, while plaat1 is thought to be responsible in other vertebrates. We used a macroevolutionary approach and comparative genomics to examine the origin, loss, synteny and selection of plaat1 across bony fishes and tetrapods. We showed that plaat1 (probably ancestral to all bony fish + tetrapods) has been lost in squamates and is significantly degraded in lineages of low-visual-acuity and blind mammals and fishes. Our findings suggest that plaat1 is important for visual acuity across bony vertebrates, and that its loss through relaxed selection and pseudogenization may have played a role in the repeated evolution of visual systems in low-light environments. Our study sheds light on the importance of gene-loss in trait evolution and provides insights into the mechanisms underlying visual acuity in low-light environments.

Multi-trait index: selection and recommendation of superior black bean genotypes as new improved varieties.

Common bean provides diet rich in vitamins, fiber, minerals, and protein, which could contribute into food security of needy populations in many countries. Developing genotypes that associate favorable agronomic and grain quality traits in the common bean crop could increase the chances of adopting new cultivars black bean. In this context, the present study aimed at selection of superior black bean lines using multi-variate indexes, Smith-Hazel-index, and genotype by yield*trait biplot analysis. These trials were conducted in Campos dos Goytacazes - RJ, in 2020 and 2021. The experimental design used was randomized blocks, with 28 treatments and three replications. The experimental unit consisted of four rows 4.0 m long, spaced at 0.50 m apart, with a sowing density of 15 seeds per meter. The two central rows were used for the evaluations. The selection of superior genotypes was conducted using the multiple trait stability index (MTSI), multi-trait genotype-ideotype distance index (MGIDI), multi-trait index based on factor analysis and genotype-ideotype distance (FAI-BLUP), Smith-Hazel index, and Genotype by Yield*Trait Biplot (GYT). The multivariate indexes efficiently selected the best black bean genotypes, presenting desirable selection gains for most traits. The use of multivariate indexes and GYT enable the selection of early genotypes with higher grain yields. These lines G9, G13, G17, G23, and G27 were selected based on their performance for multiple traits closest to the ideotype and could be recommended as new varieties.

Detecting the ecological footprint of selection.

The structure of communities is influenced by many ecological and evolutionary processes, but the way these manifest in classic biodiversity patterns often remains unclear. Here we aim to distinguish the ecological footprint of selection-through competition or environmental filtering-from that of neutral processes that are invariant to species identity. We build on existing Massive Eco-evolutionary Synthesis Simulations (MESS), which uses information from three biodiversity axes-species abundances, genetic diversity, and trait variation-to distinguish between mechanistic processes. To correctly detect and characterise competition, we add a new and more realistic form of competition that explicitly compares the traits of each pair of individuals. Our results are qualitatively different to those of previous work in which competition is based on the distance of each individual's trait to the community mean. We find that our new form of competition is easier to identify in empirical data compared to the alternatives. This is especially true when trait data are available and used in the inference procedure. Our findings hint that signatures in empirical data previously attributed to neutrality may in fact be the result of pairwise-acting selective forces. We conclude that gathering more different types of data, together with more advanced mechanistic models and inference as done here, could be the key to unravelling the mechanisms of community assembly and question the relative roles of neutral and selective processes.

Pleiotropy of positive selection in ancient ACE2 suggests an alternative hypothesis for bat-specific adaptations to host coronaviruses.

Angiotensin-convertingenzyme 2 (ACE2) has dual functions, regulating cardiovascular physiology and serving as the receptor for coronaviruses. Bats, the only true flying mammals and natural viral reservoirs, have evolved positive alterations in traits related to both functions of ACE2. This suggests significant evolutionary changes in ACE2 during bat evolution. To test this hypothesis, we examine the selection pressure in ACE2 along the ancestral branch of all bats (AncBat-ACE2), where powered flight and bat-coronavirus coevolution occurred, and detect a positive selection signature. To assess the functional effects of positive selection, we resurrect AncBat-ACE2 and its mutant (AncBat-ACE2-mut) created by replacing the positively selected sites. Compared to AncBat-ACE2-mut, AncBat-ACE2 exhibits stronger enzymatic activity, enhances mice's performance in exercise fatigue, and shows lower affinity to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Our findings indicate the functional pleiotropy of positive selection in the ancient ACE2 of bats, providing an alternative hypothesis for the evolutionary origin of bats' defense against coronaviruses.

The roles of gene duplications in the dynamics of evolutionary conflicts.

Evolutionary conflicts occur when there is antagonistic selection between different individuals of the same or different species, life stages or between levels of biological organization. Remarkably, conflicts can occur within species or within genomes. In the dynamics of evolutionary conflicts, gene duplications can play a major role because they can bring very specific changes to the genome: changes in protein dose, the generation of novel paralogues with different functions or expression patterns or the evolution of small antisense RNAs. As we describe here, by having those effects, gene duplication might spark evolutionary conflict or fuel arms race dynamics that takes place during conflicts. Interestingly, gene duplication can also contribute to the resolution of a within-locus evolutionary conflict by partitioning the functions of the gene that is under an evolutionary trade-off. In this review, we focus on intraspecific conflicts, including sexual conflict and illustrate the various roles of gene duplications with a compilation of examples. These examples reveal the level of complexity and the differences in the patterns of gene duplications within genomes under different conflicts. These examples also reveal the gene ontologies involved in conflict and the genomic location of the elements of the conflict. The examples provide a blueprint for the direct study of these conflicts or the exploration of the presence of similar conflicts in other lineages.