Comparative genomic analyses provide new insights into evolutionary history and conservation genomics of gorillas.

Genome sequencing is a powerful tool to understand species evolutionary history, uncover genes under selection, which could be informative of local adaptation, and infer measures of genetic diversity, inbreeding and mutational load that could be used to inform conservation efforts. Gorillas, critically endangered primates, have received considerable attention and with the recently sequenced Bwindi mountain gorilla population, genomic data is now available from all gorilla subspecies and both mountain gorilla populations. Here, we reanalysed this rich dataset with a focus on evolutionary history, local adaptation and genomic parameters relevant for conservation. We estimate a recent split between western and eastern gorillas of 150,000-180,000 years ago, with gene flow around 20,000 years ago, primarily between the Cross River and Grauer's gorilla subspecies. This gene flow event likely obscures evolutionary relationships within eastern gorillas: after excluding putatively introgressed genomic regions, we uncover a sister relationship between Virunga mountain gorillas and Grauer's gorillas to the exclusion of Bwindi mountain gorillas. This makes mountain gorillas paraphyletic. Eastern gorillas are less genetically diverse and more inbred than western gorillas, yet we detected lower genetic load in the eastern species. Analyses of indels fit remarkably well with differences in genetic diversity across gorilla taxa as recovered with nucleotide diversity measures. We also identified genes under selection and unique gene variants specific for each gorilla subspecies, encoding, among others, traits involved in immunity, diet, muscular development, hair morphology and behavior. The presence of this functional variation suggests that the subspecies may be locally adapted. In conclusion, using extensive genomic resources we provide a comprehensive overview of gorilla genomic diversity, including a so-far understudied Bwindi mountain gorilla population, identify putative genes involved in local adaptation, and detect population-specific gene flow across gorilla species.

Comparative transcriptomics reveals human-specific cortical features.

The cognitive abilities of humans are distinctive among primates, but their molecular and cellular substrates are poorly understood. We used comparative single-nucleus transcriptomics to analyze samples of the middle temporal gyrus (MTG) from adult humans, chimpanzees, gorillas, rhesus macaques, and common marmosets to understand human-specific features of the neocortex. Human, chimpanzee, and gorilla MTG showed highly similar cell-type composition and laminar organization as well as a large shift in proportions of deep-layer intratelencephalic-projecting neurons compared with macaque and marmoset MTG. Microglia, astrocytes, and oligodendrocytes had more-divergent expression across species compared with neurons or oligodendrocyte precursor cells, and neuronal expression diverged more rapidly on the human lineage. Only a few hundred genes showed human-specific patterning, suggesting that relatively few cellular and molecular changes distinctively define adult human cortical structure.

Ghost admixture in eastern gorillas.

Archaic admixture has had a substantial impact on human evolution with multiple events across different clades, including from extinct hominins such as Neanderthals and Denisovans into modern humans. In great apes, archaic admixture has been identified in chimpanzees and bonobos but the possibility of such events has not been explored in other species. Here, we address this question using high-coverage whole-genome sequences from all four extant gorilla subspecies, including six newly sequenced eastern gorillas from previously unsampled geographic regions. Using approximate Bayesian computation with neural networks to model the demographic history of gorillas, we find a signature of admixture from an archaic 'ghost' lineage into the common ancestor of eastern gorillas but not western gorillas. We infer that up to 3% of the genome of these individuals is introgressed from an archaic lineage that diverged more than 3 million years ago from the common ancestor of all extant gorillas. This introgression event took place before the split of mountain and eastern lowland gorillas, probably more than 40 thousand years ago and may have influenced perception of bitter taste in eastern gorillas. When comparing the introgression landscapes of gorillas, humans and bonobos, we find a consistent depletion of introgressed fragments on the X chromosome across these species. However, depletion in protein-coding content is not detectable in eastern gorillas, possibly as a consequence of stronger genetic drift in this species.

Splicing complexity as a pivotal feature of alternative exons in mammalian species.

BACKGROUND: As a significant process of post-transcriptional gene expression regulation in eukaryotic cells, alternative splicing (AS) of exons greatly contributes to the complexity of the transcriptome and indirectly enriches the protein repertoires. A large number of studies have focused on the splicing inclusion of alternative exons and have revealed the roles of AS in organ development and maturation. Notably, AS takes place through a change in the relative abundance of the transcript isoforms produced by a single gene, meaning that exons can have complex splicing patterns. However, the commonly used percent spliced-in (Ψ) values only define the usage rate of exons, but lose information about the complexity of exons' linkage pattern. To date, the extent and functional consequence of splicing complexity of alternative exons in development and evolution is poorly understood. RESULTS: By comparing splicing complexity of exons in six tissues (brain, cerebellum, heart, liver, kidney, and testis) from six mammalian species (human, chimpanzee, gorilla, macaque, mouse, opossum) and an outgroup species (chicken), we revealed that exons with high splicing complexity are prevalent in mammals and are closely related to features of genes. Using traditional machine learning and deep learning methods, we found that the splicing complexity of exons can be moderately predicted with features derived from exons, among which length of flanking exons and splicing strength of downstream/upstream splice sites are top predictors. Comparative analysis among human, chimpanzee, gorilla, macaque, and mouse revealed that, alternative exons tend to evolve to an increased level of splicing complexity and higher tissue specificity in splicing complexity. During organ development, not only developmentally regulated exons, but also 10-15% of non-developmentally regulated exons show dynamic splicing complexity. CONCLUSIONS: Our analysis revealed that splicing complexity is an important metric to characterize the splicing dynamics of alternative exons during the development and evolution of mammals.

Past Connectivity but Recent Inbreeding in Cross River Gorillas Determined Using Whole Genomes from Single Hairs.

The critically endangered western gorillas (Gorilla gorilla) are divided into two subspecies: the western lowland (G. g. gorilla) and the Cross River (G. g. diehli) gorilla. Given the difficulty in sampling wild great ape populations and the small estimated size of the Cross River gorilla population, only one whole genome of a Cross River gorilla has been sequenced to date, hindering the study of this subspecies at the population level. In this study, we expand the number of whole genomes available for wild western gorillas, generating 41 new genomes (25 belonging to Cross River gorillas) using single shed hairs collected from gorilla nests. By combining these genomes with publicly available wild gorilla genomes, we confirm that Cross River gorillas form three population clusters. We also found little variation in genome-wide heterozygosity among them. Our analyses reveal long runs of homozygosity (>10 Mb), indicating recent inbreeding in Cross River gorillas. This is similar to that seen in mountain gorillas but with a much more recent bottleneck. We also detect past gene flow between two Cross River sites, Afi Mountain Wildlife Sanctuary and the Mbe Mountains. Furthermore, we observe past allele sharing between Cross River gorillas and the northern western lowland gorilla sites, as well as with the eastern gorilla species. This is the first study using single shed hairs from a wild species for whole genome sequencing to date. Taken together, our results highlight the importance of implementing conservation measures to increase connectivity among Cross River gorilla sites.

Gene Content and Coding Diversity of the Growth Hormone Loci of Apes.

The growth hormone (GH) locus has experienced a dramatic evolution in primates, becoming multigenic and diverse in anthropoids. Despite sequence information from a vast number of primate species, it has remained unclear how the multigene family was favored. We compared the structure and composition of apes' GH loci as a prerequisite to understanding their origin and possible evolutionary role. These thorough analyses of the GH loci of the chimpanzee, gorilla, and orangutan were done by resorting to previously sequenced bacterial artificial chromosomes (BACs) harboring them, as well as to their respective genome projects data available in GenBank. The GH loci of modern man, Neanderthal, gibbon, and wild boar were retrieved from GenBank. Coding regions, regulatory elements, and repetitive sequences were identified and compared among species. The GH loci of all the analyzed species are flanked by the genes CD79B (5') and ICAM-1 (3'). In man, Neanderthal, and chimpanzee, the loci were integrated by five almost indistinguishable genes; however, in the former two, they rendered three different hormones, and in the latter, four different proteins were derived. Gorilla exhibited six genes, gibbon seven, and orangutan four. The sequences of the proximal promoters, enhancers, P-elements, and a locus control region (LCR) were highly conserved. The locus evolution might have implicated duplications of the ancestral pituitary gene (GH-N) and subsequent diversification of the copies, leading to the placental single GH-V gene and the multiple CSH genes.

Simian homologues of human herpesviruses and implications for novel viral introduction to free-living mountain gorillas.

The endangered mountain gorilla (Gorilla beringei beringei) in Rwanda, Uganda, and the Democratic Republic of Congo is frequently in contact with humans through tourism, research activities, and illegal entry of people into protected gorilla habitat. Herpesviruses, which are ubiquitous in primates, have the potential to be shared in any setting where humans and gorillas share habitat. Based on serological findings and clinical observations of orofacial ulcerated lesions resembling herpetic lesions, an alpha-herpesvirus resembling human herpes simplex virus type 1 (HSV-1) has long been suspected to be present in human-habituated mountain gorillas in the wild. While the etiology of orofacial lesions in the wild has not been confirmed, HSV-1 has been suspected in captively-housed mountain gorillas and confirmed in a co-housed confiscated Grauer's gorilla (Gorilla beringei graueri). To better characterize herpesviruses infecting mountain gorillas and to determine the presence/absence of HSV-1 in the free-living population, we conducted a population-wide survey to test for the presence of orally shed herpesviruses. DNA was extracted from discarded chewed plants collected from 294 individuals from 26 groups, and samples were screened by polymerase chain reaction using pan-herpesvirus and HSV-1-specific assays. We found no evidence that human herpesviruses had infected free-ranging mountain gorillas. However, we found gorilla-specific homologs to human herpesviruses, including cytomegaloviruses (GbbCMV-1 and 2), a lymphocryptovirus (GbbLCV-1), and a new rhadinovirus (GbbRHV-1) with similar characteristics (i.e., timing of primary infection, shedding in multiple age groups, and potential modes of transmission) to their human counterparts, human cytomegalovirus, Epstein-Barr virus and Kaposi's sarcoma-associated herpesvirus, respectively.

Isolated Grauer's gorilla populations differ in diet and gut microbiome.

The animal gut microbiome has been implicated in a number of key biological processes, ranging from digestion to behaviour, and has also been suggested to facilitate local adaptation. Yet studies in wild animals rarely compare multiple populations that differ ecologically, which is the level at which local adaptation may occur. Further, few studies simultaneously characterize diet and gut microbiome from the same sample, despite their probable interdependence. Here, we investigate the interplay between diet and gut microbiome in three geographically isolated populations of the critically endangered Grauer's gorilla (Gorilla beringei graueri), which we show to be genetically differentiated. We find population- and social group-specific dietary and gut microbial profiles and covariation between diet and gut microbiome, despite the presence of core microbial taxa. There was no detectable effect of age, and only marginal effects of sex and genetic relatedness on the microbiome. Diet differed considerably across populations, with the high-altitude population consuming a lower diversity of plants compared to low-altitude populations, consistent with plant availability constraining dietary choices. The observed pattern of covariation between diet and gut microbiome is probably a result of long-term social and environmental factors. Our study suggests that the gut microbiome is sufficiently plastic to support flexible food selection and hence contribute to local adaptation.

Global abundance of short tandem repeats is non-random in rodents and primates.

BACKGROUND: While of predominant abundance across vertebrate genomes and significant biological implications, the relevance of short tandem repeats (STRs) (also known as microsatellites) to speciation remains largely elusive and attributed to random coincidence for the most part. Here we collected data on the whole-genome abundance of mono-, di-, and trinucleotide STRs in nine species, encompassing rodents and primates, including rat, mouse, olive baboon, gelada, macaque, gorilla, chimpanzee, bonobo, and human. The collected data were used to analyze hierarchical clustering of the STR abundances in the selected species. RESULTS: We found massive differential STR abundances between the rodent and primate orders. In addition, while numerous STRs had random abundance across the nine selected species, the global abundance conformed to three consistent < clusters>, as follows: <rat, mouse>, <gelada, macaque, olive baboon>, and <gorilla, chimpanzee, bonobo, human>, which coincided with the phylogenetic distances of the selected species (p < 4E-05). Exceptionally, in the trinucleotide STR compartment, human was significantly distant from all other species. CONCLUSION: Based on hierarchical clustering, we propose that the global abundance of STRs is non-random in rodents and primates, and probably had a determining impact on the speciation of the two orders. We also propose the STRs and STR lengths, which predominantly conformed to the phylogeny of the selected species, exemplified by (t)10, (ct)6, and (taa4). Phylogenetic and experimental platforms are warranted to further examine the observed patterns and the biological mechanisms associated with those STRs.

Human-specific regulation of neural maturation identified by cross-primate transcriptomics.

Unique aspects of human behavior are often attributed to differences in the relative size and organization of the human brain: these structural aspects originate during early development. Recent studies indicate that human neurodevelopment is considerably slower than that in other nonhuman primates, a finding that is termed neoteny. One aspect of neoteny is the slow onset of action potentials. However, which molecular mechanisms play a role in this process remain unclear. To examine the evolutionary constraints on the rate of neuronal maturation, we have generated transcriptional data tracking five time points, from the neural progenitor state to 8-week-old neurons, in primates spanning the catarrhine lineage, including Macaca mulatta, Gorilla gorilla, Pan paniscus, Pan troglodytes, and Homo sapiens. Despite finding an overall similarity of many transcriptional signatures, species-specific and clade-specific distinctions were observed. Among the genes that exhibited human-specific regulation, we identified a key pioneer transcription factor, GATA3, that was uniquely upregulated in humans during the neuronal maturation process. We further examined the regulatory nature of GATA3 in human cells and observed that downregulation quickened the speed of developing spontaneous action potentials, thereby modulating the human neotenic phenotype. These results provide evidence for the divergence of gene regulation as a key molecular mechanism underlying human neoteny.

Milk microbiomes of three great ape species vary among host species and over time.

In mammalian neonates, milk consumption provides nutrients, growth factors, immune molecules, and microbes. Milk microbiomes are increasingly recognized for their roles in seeding infant gut microbiomes and priming immune development. However, milk microbiome variation within and among individuals remains under investigation. We used 16S rRNA gene sequencing to investigate factors shaping milk microbiomes in three captive great ape species: Gorilla gorilla gorilla (individuals, N = 4; samples, n = 29), Pongo abelii (N = 2; n = 16), and Pongo pygmaeus (N = 1; n = 9). We demonstrate variation among host species, over lactation, and between housing facilities. In phylogenetic community composition, milk microbiomes were distinct among the three ape species. We found only a few shared, abundant bacterial taxa and suggest that they likely serve functional roles. The diversity and community composition of milk microbiomes showed gradual changes over time in gorillas and the Bornean orangutan, which was detectable with our comprehensive sampling over lactation stages (> 300-day span). In gorillas, milk microbiomes differed between housing facilities, but were similar between dams within a facility. These results support the strong influence of evolutionary history in shaping milk microbiomes, but also indicate that more proximate cues from mother, offspring, and the environment affect the distribution of rarer microbial taxa.

Gastrointestinal symbiont diversity in wild gorilla: A comparison of bacterial and strongylid communities across multiple localities.

Western lowland gorillas (Gorilla gorilla gorilla) are Critically Endangered and show continued population decline. Consequently, pressure is mounting to better understand their conservation threats and ecology. Gastrointestinal symbionts, such as bacterial and eukaryotic communities, are believed to play vital roles in the physiological landscape of the host. Gorillas host a broad spectrum of eucaryotes, so called parasites, with strongylid nematodes being particularly prevalent. While these communities are partially consistent, they are also shaped by various ecological factors, such as diet or habitat type. To investigate gastrointestinal symbionts of wild western lowland gorillas, we analysed 215 faecal samples from individuals in five distinct localities across the Congo Basin, using high-throughput sequencing techniques. We describe the gut bacterial microbiome and genetic diversity of strongylid communities, including strain-level identification of amplicon sequence variants (ASVs). We identified strongylid ASVs from eight genera and bacterial ASVs from 20 phyla. We compared these communities across localities, with reference to varying environmental factors among populations, finding differences in alpha diversity and community compositions of both gastrointestinal components. Moreover, we also investigated covariation between strongylid nematodes and the bacterial microbiome, finding correlations between strongylid taxa and Prevotellaceae and Rikenellaceae ASVs that were consistent across multiple localities. Our research highlights the complexity of the bacterial microbiome and strongylid communities in several gorilla populations and emphasizes potential interactions between these two symbiont communities. This study provides a framework for ongoing research into strongylid nematode diversity, and their interactions with the bacterial microbiome, among great apes.

Fragmented mitochondrial genomes of seal lice (family Echinophthiriidae) and gorilla louse (family Pthiridae): frequent minichromosomal splits and a host switch of lice between seals.

BACKGROUND: The mitochondrial (mt) genomes of 15 species of sucking lice from seven families have been studied to date. These louse species have highly dynamic, fragmented mt genomes that differ in the number of minichromosomes, the gene content, and gene order in a minichromosome between families and even between species of the same genus. RESULTS: In the present study, we analyzed the publicly available data to understand mt genome fragmentation in seal lice (family Echinophthiriidae) and gorilla louse, Pthirus gorillae (family Pthiridae), in particular the role of minichromosome split and minichromosome merger in the evolution of fragmented mt genomes. We show that 1) at least three ancestral mt minichromosomes of sucking lice have split in the lineage leading to seal lice, 2) one minichromosome ancestral to primate lice has split in the lineage to the gorilla louse, and 3) two ancestral minichromosomes of seal lice have merged in the lineage to the northern fur seal louse. Minichromosome split occurred 15-16 times in total in the lineages leading to species in six families of sucking lice investigated. In contrast, minichromosome merger occurred only four times in the lineages leading to species in three families of sucking lice. Further, three ancestral mt minichromosomes of sucking lice have split multiple times independently in different lineages of sucking lice. Our analyses of mt karyotypes and gene sequences also indicate the possibility of a host switch of crabeater seal louse to Weddell seals. CONCLUSIONS: We conclude that: 1) minichromosome split contributes more than minichromosome merger in mt genome fragmentation of sucking lice, and 2) mt karyotype comparison helps understand the phylogenetic relationships between sucking louse species.

Facial asymmetry tracks genetic diversity among Gorilla subspecies.

Mountain gorillas are particularly inbred compared to other gorillas and even the most inbred human populations. As mountain gorilla skeletal material accumulated during the 1970s, researchers noted their pronounced facial asymmetry and hypothesized that it reflects a population-wide chewing side preference. However, asymmetry has also been linked to environmental and genetic stress in experimental models. Here, we examine facial asymmetry in 114 crania from three Gorilla subspecies using 3D geometric morphometrics. We measure fluctuating asymmetry (FA), defined as random deviations from perfect symmetry, and population-specific patterns of directional asymmetry (DA). Mountain gorillas, with a current population size of about 1000 individuals, have the highest degree of facial FA (explaining 17% of total facial shape variation), followed by Grauer gorillas (9%) and western lowland gorillas (6%), despite the latter experiencing the greatest ecological and dietary variability. DA, while significant in all three taxa, explains relatively less shape variation than FA does. Facial asymmetry correlates neither with tooth wear asymmetry nor increases with age in a mountain gorilla subsample, undermining the hypothesis that facial asymmetry is driven by chewing side preference. An examination of temporal trends shows that stress-induced developmental instability has increased over the last 100 years in these endangered apes.

The complex Y-chromosomal history of gorillas.

Studies of the evolutionary relationships among gorilla populations using autosomal and mitochondrial sequences suggest that male-mediated gene flow may have been important in the past, but data on the Y-chromosomal relationships among the gorilla subspecies are limited. Here, we genotyped blood and noninvasively collected fecal samples from 12 captives and 257 wild male gorillas of known origin representing all four subspecies (Gorilla gorilla gorilla, G. g. diehli, G. beringei beringei, and G. b. graueri) at 10 Y-linked microsatellite loci resulting in 102 unique Y-haplotypes for 224 individuals. We found that western lowland gorilla (G. g. gorilla) haplotypes were consistently more diverse than any other subspecies for all measures of diversity and comprised several genetically distinct groups. However, these did not correspond to geographical proximity and some closely related haplotypes were found several hundred kilometers apart. Similarly, our broad sampling of eastern gorillas revealed that mountain (G. b. beringei) and Grauer's (G. b. graueri) gorilla Y-chromosomal haplotypes did not form distinct clusters. These observations suggest structure in the ancestral population with subsequent mixing of differentiated haplotypes by male dispersal for western lowland gorillas, and postisolation migration or incomplete lineage sorting due to short divergence times for eastern gorillas.

The genetic impact of an Ebola outbreak on a wild gorilla population.

BACKGROUND: Numerous Ebola virus outbreaks have occurred in Equatorial Africa over the past decades. Besides human fatalities, gorillas and chimpanzees have also succumbed to the fatal virus. The 2004 outbreak at the Odzala-Kokoua National Park (Republic of Congo) alone caused a severe decline in the resident western lowland gorilla (Gorilla gorilla gorilla) population, with a 95% mortality rate. Here, we explore the immediate genetic impact of the Ebola outbreak in the western lowland gorilla population. RESULTS: Associations with survivorship were evaluated by utilizing DNA obtained from fecal samples from 16 gorilla individuals declared missing after the outbreak (non-survivors) and 15 individuals observed before and after the epidemic (survivors). We used a target enrichment approach to capture the sequences of 123 genes previously associated with immunology and Ebola virus resistance and additionally analyzed the gut microbiome which could influence the survival after an infection. Our results indicate no changes in the population genetic diversity before and after the Ebola outbreak, and no significant differences in microbial community composition between survivors and non-survivors. However, and despite the low power for an association analysis, we do detect six nominally significant missense mutations in four genes that might be candidate variants associated with an increased chance of survival. CONCLUSION: This study offers the first insight to the genetics of a wild great ape population before and after an Ebola outbreak using target capture experiments from fecal samples, and presents a list of candidate loci that may have facilitated their survival.

A comprehensive analysis of gorilla-specific LINE-1 retrotransposons.

BACKGROUND: Long interspersed element-1 (LINE-1 or L1) is the most abundant retrotransposons in the primate genome. They have approximately 520,000 copies and make up ~ 17% of the primate genome. Full-length L1s can mobilize to a new genomic location using their enzymatic machinery. Gorilla is the second closest species to humans after the chimpanzee, and human-gorilla split 7-12 million years ago. The gorilla genome provides an opportunity to explore primate origins and evolution. OBJECTIVE: L1s have contributed to genome diversity and variations during primate evolution. This study aimed to identify gorilla-specific L1s using a more recent version of the gorilla reference genome (Mar. 2016 GSMRT3/gorGor5). METHODS: We collected gorilla-specific L1 candidates through computational analysis and manual inspection. L1Xplorer was used to identify whether full-length gorilla-specific L1s were intact. In addition, to determine the level of sequence conservation between intact fulllength gorilla-specific L1s, two ORFs of intact L1s were aligned with the L1PA2 consensus sequence. RESULTS: 2002 gorilla-specific L1 candidates were identified through computational analysis. Among them, we manually inspected 1,883 gorilla-specific L1s, among which most of them belong to the L1PA2 subfamily and 12 were intact L1s that could influence genomic variations in the gorilla genome. Interestingly, the 12 intact full-length gorilla-specific L1s have 14 highly conserved nonsynonymous mutations, including 6 mutations and 8 mutations in ORF1 and ORF2, respectively. In comparison to the intact full-length chimpanzee-specific L1s and human-specific hot-L1s, two of these in ORF1 (L256F and E293G) were shown as gorilla-specific nonsynonymous mutations. CONCLUSION: The gorilla-specific L1s may have had significantly affected the gorilla genome to compose a genome different form that of other primates during primate evolution.

A high-quality bonobo genome refines the analysis of hominid evolution.

The divergence of chimpanzee and bonobo provides one of the few examples of recent hominid speciation1,2. Here we describe a fully annotated, high-quality bonobo genome assembly, which was constructed without guidance from reference genomes by applying a multiplatform genomics approach. We generate a bonobo genome assembly in which more than 98% of genes are completely annotated and 99% of the gaps are closed, including the resolution of about half of the segmental duplications and almost all of the full-length mobile elements. We compare the bonobo genome to those of other great apes1,3-5 and identify more than 5,569 fixed structural variants that specifically distinguish the bonobo and chimpanzee lineages. We focus on genes that have been lost, changed in structure or expanded in the last few million years of bonobo evolution. We produce a high-resolution map of incomplete lineage sorting and estimate that around 5.1% of the human genome is genetically closer to chimpanzee or bonobo and that more than 36.5% of the genome shows incomplete lineage sorting if we consider a deeper phylogeny including gorilla and orangutan. We also show that 26% of the segments of incomplete lineage sorting between human and chimpanzee or human and bonobo are non-randomly distributed and that genes within these clustered segments show significant excess of amino acid replacement compared to the rest of the genome.

Hovlinc is a recently evolved class of ribozyme found in human lncRNA.

Although naturally occurring catalytic RNA molecules-ribozymes-have attracted a great deal of research interest, very few have been identified in humans. Here, we developed a genome-wide approach to discovering self-cleaving ribozymes and identified a naturally occurring ribozyme in humans. The secondary structure and biochemical properties of this ribozyme indicate that it belongs to an unidentified class of small, self-cleaving ribozymes. The sequence of the ribozyme exhibits a clear evolutionary path, from its appearance between ~130 and ~65 million years ago (Ma), to acquiring self-cleavage activity very recently, ~13-10 Ma, in the common ancestors of humans, chimpanzees and gorillas. The ribozyme appears to be functional in vivo and is embedded within a long noncoding RNA belonging to a class of very long intergenic noncoding RNAs. The presence of a catalytic RNA enzyme in lncRNA creates the possibility that these transcripts could function by carrying catalytic RNA domains.

Dynamic evolution of great ape Y chromosomes.

The mammalian male-specific Y chromosome plays a critical role in sex determination and male fertility. However, because of its repetitive and haploid nature, it is frequently absent from genome assemblies and remains enigmatic. The Y chromosomes of great apes represent a particular puzzle: their gene content is more similar between human and gorilla than between human and chimpanzee, even though human and chimpanzee share a more recent common ancestor. To solve this puzzle, here we constructed a dataset including Ys from all extant great ape genera. We generated assemblies of bonobo and orangutan Ys from short and long sequencing reads and aligned them with the publicly available human, chimpanzee, and gorilla Y assemblies. Analyzing this dataset, we found that the genus Pan, which includes chimpanzee and bonobo, experienced accelerated substitution rates. Pan also exhibited elevated gene death rates. These observations are consistent with high levels of sperm competition in Pan Furthermore, we inferred that the great ape common ancestor already possessed multicopy sequences homologous to most human and chimpanzee palindromes. Nonetheless, each species also acquired distinct ampliconic sequences. We also detected increased chromatin contacts between and within palindromes (from Hi-C data), likely facilitating gene conversion and structural rearrangements. Our results highlight the dynamic mode of Y chromosome evolution and open avenues for studies of male-specific dispersal in endangered great ape species.