Relationships between the hard and soft dimensions of the nose in Pan troglodytes and Homo sapiens reveal the positions of the nasal tips of Plio-Pleistocene hominids.

By identifying homogeneity in bone and soft tissue covariation patterns in living hominids, it is possible to produce facial approximation methods with interspecies compatibility. These methods may be useful for producing facial approximations of fossil hominids that are more realistic than currently possible. In this study, we conducted an interspecific comparison of the nasomaxillary region in chimpanzees and modern humans with the aim of producing a method for predicting the positions of the nasal tips of Plio-Pleistocene hominids. We addressed this aim by first collecting and performing regression analyses of linear and angular measurements of nasal cavity length and inclination in modern humans (Homo sapiens; n = 72) and chimpanzees (Pan troglodytes; n = 19), and then performing a set of out-of-group tests. The first test was performed on four subjects that belonged to the same genus as the training sample, i.e., Homo (n = 2) and Pan (n = 2), and the second test, which functioned as an interspecies compatibility test, was performed on Pan paniscus (n = 1), Gorilla gorilla (n = 3), Pongo pygmaeus (n = 1), Pongo abelli (n = 1), Symphalangus syndactylus (n = 3), and Papio hamadryas (n = 3). We identified statistically significant correlations in both humans and chimpanzees with slopes that displayed homogeneity of covariation. Prediction formulae combining these data were found to be compatible with humans and chimpanzees as well as all other African great apes, i.e., bonobos and gorillas. The main conclusion that can be drawn from this study is that our set of regression models for approximating the position of the nasal tip are homogenous among humans and African apes, and can thus be reasonably extended to ancestors leading to these clades.

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.

GC and Repeats Profiling along Chromosomes-The Future of Fish Compositional Cytogenomics.

The study of fish cytogenetics has been impeded by the inability to produce G-bands that could assign chromosomes to their homologous pairs. Thus, the majority of karyotypes published have been estimated based on morphological similarities of chromosomes. The reason why chromosome G-banding does not work in fish remains elusive. However, the recent increase in the number of fish genomes assembled to the chromosome level provides a way to analyse this issue. We have developed a Python tool to visualize and quantify GC percentage (GC%) of both repeats and unique DNA along chromosomes using a non-overlapping sliding window approach. Our tool profiles GC% and simultaneously plots the proportion of repeats (rep%) in a color scale (or vice versa). Hence, it is possible to assess the contribution of repeats to the total GC%. The main differences are the GC% of repeats homogenizing the overall GC% along fish chromosomes and a greater range of GC% scattered along fish chromosomes. This may explain the inability to produce G-banding in fish. We also show an occasional banding pattern along the chromosomes in some fish that probably cannot be detected with traditional qualitative cytogenetic methods.

Application of the geographic population structure (GPS) algorithm for biogeographical analyses of wild and captive gorillas.

BACKGROUND: The utilization of high resolution genome data has important implications for the phylogeographical evaluation of non-human species. Biogeographical analyses can yield detailed understanding of their population biology and facilitate the geo-localization of individuals to promote their efficacious management, particularly when bred in captivity. The Geographic Population Structure (GPS) algorithm is an admixture based tool for inference of biogeographical affinities and has been employed for the geo-localization of various human populations worldwide. Here, we applied the GPS tool for biogeographical analyses and localization of the ancestral origins of wild and captive gorilla genomes, of unknown geographic source, available in the Great Ape Genome Project (GAGP), employing Gorillas with known ancestral origin as the reference data. RESULTS: Our findings suggest that GPS was successful in recapitulating the population history and estimating the geographic origins of all gorilla genomes queried and localized the wild gorillas with unknown geographical origin < 150 km of National Parks/Wildlife Reserves within the political boundaries of countries, considered as prominent modern-day abode for gorillas in the wild. Further, the GPS localization of most captive-born gorillas was congruent with their previously presumed ancestral homes. CONCLUSIONS: Currently there is limited knowledge of the ancestral origins of most North American captive gorillas, and our study highlights the usefulness of GPS for inferring ancestry of captive gorillas. Determination of the native geographical source of captive gorillas can provide valuable information to guide breeding programs and ensure their appropriate management at the population level. Finally, our findings shine light on the broader applicability of GPS for protecting the genetic integrity of other endangered non-human species, where controlled breeding is a vital component of their conservation.

Discovery of gorilla MHC-C expressing C1 ligand for KIR.

In comparison to humans and chimpanzees, gorillas show low diversity at MHC class I genes (Gogo), as reflected by an overall reduced level of allelic variation as well as the absence of a functionally important sequence motif that interacts with killer cell immunoglobulin-like receptors (KIR). Here, we use recently generated large-scale genomic sequence data for a reassessment of allelic diversity at Gogo-C, the gorilla orthologue of HLA-C. Through the combination of long-range amplifications and long-read sequencing technology, we obtained, among the 35 gorillas reanalyzed, three novel full-length genomic sequences including a coding region sequence that has not been previously described. The newly identified Gogo-C*03:01 allele has a divergent recombinant structure that sets it apart from other Gogo-C alleles. Domain-by-domain phylogenetic analysis shows that Gogo-C*03:01 has segments in common with Gogo-B*07, the additional B-like gene that is present on some gorilla MHC haplotypes. Identified in ~ 50% of the gorillas analyzed, the Gogo-C*03:01 allele exclusively encodes the C1 epitope among Gogo-C allotypes, indicating its important function in controlling natural killer cell (NK cell) responses via KIR. We further explored the hypothesis whether gorillas experienced a selective sweep which may have resulted in a general reduction of the gorilla MHC class I repertoire. Our results provide little support for a selective sweep but rather suggest that the overall low Gogo class I diversity can be best explained by drastic demographic changes gorillas experienced in the ancient and recent past.

Gorilla MHC class I gene and sequence variation in a comparative context.

Comparisons of MHC gene content and diversity among closely related species can provide insights into the evolutionary mechanisms shaping immune system variation. After chimpanzees and bonobos, gorillas are humans' closest living relatives; but in contrast, relatively little is known about the structure and variation of gorilla MHC class I genes (Gogo). Here, we combined long-range amplifications and long-read sequencing technology to analyze full-length MHC class I genes in 35 gorillas. We obtained 50 full-length genomic sequences corresponding to 15 Gogo-A alleles, 4 Gogo-Oko alleles, 21 Gogo-B alleles, and 10 Gogo-C alleles including 19 novel coding region sequences. We identified two previously undetected MHC class I genes related to Gogo-A and Gogo-B, respectively, thereby illustrating the potential of this approach for efficient and highly accurate MHC genotyping. Consistent with their phylogenetic position within the hominid family, individual gorilla MHC haplotypes share characteristics with humans and chimpanzees as well as orangutans suggesting a complex history of the MHC class I genes in humans and the great apes. However, the overall MHC class I diversity appears to be low further supporting the hypothesis that gorillas might have experienced a reduction of their MHC repertoire.

Geographic variation in gorilla limb bones.

Gorilla systematics has received increased attention over recent decades from primatologists, conservationists, and paleontologists. Studies of geographic variation in DNA, skulls, and teeth have led to new taxonomic proposals, such as recognition of two gorilla species, Gorilla gorilla (western gorilla) and Gorilla beringei (eastern gorilla). Postcranial differences between mountain gorillas (G. beringei beringei) and western lowland gorillas (G. g. gorilla) have a long history of study, but differences between the limb bones of the eastern and western species have not yet been examined with an emphasis on geographic variation within each species. In addition, proposals for recognition of the Cross River gorilla as Gorilla gorilla diehli and gorillas from Tshiaberimu and Kahuzi as G. b. rex-pymaeorum have not been evaluated in the context of geographic variation in the forelimb and hindlimb skeletons. Forty-three linear measurements were collected from limb bones of 266 adult gorillas representing populations of G. b. beringei, Gorilla beringei graueri, G. g. gorilla, and G. g. diehli in order to investigate geographic diversity. Skeletal elements included the humerus, radius, third metacarpal, third proximal hand phalanx, femur, tibia, calcaneus, first metatarsal, third metatarsal, and third proximal foot phalanx. Comparisons of means and principal components analyses clearly differentiate eastern and western gorillas, indicating that eastern gorillas have absolutely and relatively smaller hands and feet, among other differences. Gorilla subspecies and populations cluster consistently by species, although G. g. diehli may be similar to the eastern gorillas in having small hands and feet. The subspecies of G. beringei are distinguished less strongly and by different variables than the two gorilla species. Populations of G. b. graueri are variable, and Kahuzi and Tshiaberimu specimens do not cluster together. Results support the possible influence of higher-altitude Pleistocene refugia on patterns of geographic variation in gorillas.

The evolutionary origin and population history of the grauer gorilla.

Gorillas living in western central Africa (Gorilla gorilla) are morphologically and genetically distinguishable from those living in eastern central Africa (Gorilla beringei). Genomic analyses show eastern gorillas experienced a significant reduction in population size during the Pleistocene subsequent to geographical isolation from their western counterparts. However, how these results relate more specifically to the recent biogeographical and evolutionary history of eastern gorillas remains poorly understood. Here we show that two rare morphological traits are present in the hands and feet of both eastern gorilla subspecies at strikingly high frequencies (>60% in G. b. graueri; ∼28% in G. b. beringei) in comparison with western gorillas (<1%). The intrageneric distribution of these rare traits suggests that they became common among eastern gorillas after diverging from their western relatives during the early to middle Pleistocene. The extremely high frequencies observed among grauer gorillas-which currently occupy a geographic range more than ten times the size of that of mountain gorillas-imply that grauers originated relatively recently from a small founding population of eastern gorillas. Current paleoenvironmental, geological, and biogeographical evidence supports the hypothesis that a small group of eastern gorillas likely dispersed westward from the Virungas into present-day grauer range in the highlands just north of Lake Kivu, either immediately before or directly after the Younger Dryas interval. We propose that as the lowland forests of central Africa expanded rapidly during the early Holocene, they became connected with the expanding highland forests along the Albertine Rift and enabled the descendants of this small group to widely disperse. The descendant populations significantly expanded their geographic range and population numbers relative to the gorillas of the Virunga Mountains and the Bwindi-Impenetrable Forest, ultimately resulting in the grauer gorilla subspecies recognized today. This founder-effect hypothesis offers some optimism for modern conservation efforts to save critically endangered eastern gorillas from extinction.

The complete mitochondrial genome of eastern lowland gorilla, Gorilla beringei graueri, and comparative mitochondrial genomics of Gorilla species.

In this study, we determined the complete mitochondrial (mt) genome of eastern lowland gorilla, Gorilla beringei graueri for the first time. The total genome was 16,416 bp in length. It contained a total of 13 protein-coding genes, 22 transfer RNA genes, 2 ribosomal RNA genes and 1 control region (D-loop region). The base composition was A (30.88%), G (13.10%), C (30.89%) and T (25.13%), indicating that the percentage of A+T (56.01%) was higher than G+C (43.99%). Comparisons with the other publicly available Gorilla mitogenome showed the conservation of gene order and base compositions but a bunch of nucleotide diversity. This complete mitochondrial genome sequence will provide valuable genetic information for further studies on conservation genetics of eastern lowland gorilla.

Characterization of MHC class II B polymorphism in multiple populations of wild gorillas using non-invasive samples and next-generation sequencing.

Genes encoded by the major histocompatibility complex (MHC) are crucial for the recognition and presentation of antigens to the immune system. In contrast to their closest relatives, chimpanzees and humans, much less is known about variation in gorillas at these loci. This study explored the exon 2 variation of -DPB1, -DQB1, and -DRB genes in 46 gorillas from four populations while simultaneously evaluating the feasibility of using fecal samples for high-throughput MHC genotyping. By applying strict similarity- and frequency-based analysis, we found, despite our modest sample size, a total of 18 alleles that have not been described previously, thereby illustrating the potential for efficient and highly accurate MHC genotyping from non-invasive DNA samples. We emphasize the importance of controlling for multiple potential sources of error when applying this massively parallel short-read sequencing technology to PCR products generated from low concentration DNA extracts. We observed pronounced differences in MHC variation between species, subspecies and populations that are consistent with both the ancient and recent demographic histories experienced by gorillas.

Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding.

Mountain gorillas are an endangered great ape subspecies and a prominent focus for conservation, yet we know little about their genomic diversity and evolutionary past. We sequenced whole genomes from multiple wild individuals and compared the genomes of all four Gorilla subspecies. We found that the two eastern subspecies have experienced a prolonged population decline over the past 100,000 years, resulting in very low genetic diversity and an increased overall burden of deleterious variation. A further recent decline in the mountain gorilla population has led to extensive inbreeding, such that individuals are typically homozygous at 34% of their sequence, leading to the purging of severely deleterious recessive mutations from the population. We discuss the causes of their decline and the consequences for their future survival.

Inference of gorilla demographic and selective history from whole-genome sequence data.

Although population-level genomic sequence data have been gathered extensively for humans, similar data from our closest living relatives are just beginning to emerge. Examination of genomic variation within great apes offers many opportunities to increase our understanding of the forces that have differentially shaped the evolutionary history of hominid taxa. Here, we expand upon the work of the Great Ape Genome Project by analyzing medium to high coverage whole-genome sequences from 14 western lowland gorillas (Gorilla gorilla gorilla), 2 eastern lowland gorillas (G. beringei graueri), and a single Cross River individual (G. gorilla diehli). We infer that the ancestors of western and eastern lowland gorillas diverged from a common ancestor approximately 261 ka, and that the ancestors of the Cross River population diverged from the western lowland gorilla lineage approximately 68 ka. Using a diffusion approximation approach to model the genome-wide site frequency spectrum, we infer a history of western lowland gorillas that includes an ancestral population expansion of 1.4-fold around 970 ka and a recent 5.6-fold contraction in population size 23 ka. The latter may correspond to a major reduction in African equatorial forests around the Last Glacial Maximum. We also analyze patterns of variation among western lowland gorillas to identify several genomic regions with strong signatures of recent selective sweeps. We find that processes related to taste, pancreatic and saliva secretion, sodium ion transmembrane transport, and cardiac muscle function are overrepresented in genomic regions predicted to have experienced recent positive selection.

Three-dimensional geometric morphometric analysis of talar morphology in extant gorilla taxa from highland and lowland habitats.

Western gorillas (Gorilla gorilla) are known to climb significantly more often than eastern gorillas (Gorilla beringei), a behavioral distinction attributable to major differences in their respective habitats (i.e., highland vs. lowland). Genetic evidence suggests that the lineages leading to these taxa began diverging from one another between approximately 1 and 3 million years ago. Thus, gorillas offer a special opportunity to examine the degree to which morphology of recently diverged taxa may be "fine-tuned" to differing ecological requirements. Using three-dimensional (3D) geometric morphometrics, we compared talar morphology in a sample of 87 specimens including western (lowland), mountain (highland), and grauer gorillas (lowland and highland populations). Talar shape was captured with a series of landmarks and semilandmarks superimposed by generalized Procrustes analysis. A between-group principal components analysis of overall talar shape separates gorillas by ecological habitat and by taxon. An analysis of only the trochlea and lateral malleolar facet identifies subtle variations in trochlear shape between western lowland and lowland grauer gorillas, potentially indicative of convergent evolution of arboreal adaptations in the talus. Lastly, talar shape scales differently with centroid size for highland and lowland gorillas, suggesting that ankle morphology may track body-size mediated variation in arboreal behaviors differently depending on ecological setting. Several of the observed shape differences are linked biomechanically to the facilitation of climbing in lowland gorillas and to stability and load-bearing on terrestrial substrates in the highland taxa, providing an important comparative model for studying morphological variation in groups known only from fossils (e.g., early hominins).

Hypothesis: brain size and skull shape as criteria for a new hominin family tree.

Today, gorillas and chimpanzees live in tropical forests, where acid soils do not favor fossilization. It is thus widely believed that there are no fossils of chimpanzees or gorillas. However, four teeth of a 0.5-million-year (Ma)-old chimpanzee were discovered in the rift valley of Kenya (McBrearty and Jablonski, 2005), and a handful of teeth of a 10-Ma-old gorilla-like creature were found in Ethiopia (Suwa et al., 2007), close to the major sites of Homo discoveries. These discoveries indicate that chimpanzees and gorillas once shared their range with early Homo. However, the thousands of hominin fossils discovered in the past century have all been attributed to the Homo line. Thus far, our family tree looks like a bush with many dead-branches. If one admits the possibility that the australopithecines can also be the ancestors of African great apes, one can place Paranthropus on the side of gorilla ancestors and divide the remaining Australopithecus based on the brain size into the two main lines of humans and chimpanzees, thereby resulting in a coherent family tree.

Variance in the reproductive success of dominant male mountain gorillas.

Using 30 years of demographic data from 15 groups, this study estimates how harem size, female fertility, and offspring survival may contribute to variance in the siring rates of dominant male mountain gorillas throughout the Virunga Volcano Region. As predicted for polygynous species, differences in harem size were the greatest source of variance in the siring rate, whereas differences in female fertility and offspring survival were relatively minor. Harem size was positively correlated with offspring survival, even after removing all known and suspected cases of infanticide, so the correlation does not seem to reflect differences in the ability of males to protect their offspring. Harem size was not significantly correlated with female fertility, which is consistent with the hypothesis that mountain gorillas have minimal feeding competition. Harem size, offspring survival, and siring rates were not significantly correlated with the proportion of dominant tenures that occurred in multimale groups versus one-male groups; even though infanticide is less likely when those tenures end in multimale groups than one-male groups. In contrast with the relatively small contribution of offspring survival to variance in the siring rates of this study, offspring survival is a major source of variance in the male reproductive success of western gorillas, which have greater predation risks and significantly higher rates of infanticide. If differences in offspring protection are less important among male mountain gorillas than western gorillas, then the relative importance of other factors may be greater for mountain gorillas. Thus, our study illustrates how variance in male reproductive success and its components can differ between closely related species.

Ectocranial suture fusion in primates: pattern and phylogeny.

Patterns of ectocranial suture fusion among Primates are subject to species-specific variation. In this study, we used Guttman Scaling to compare modal progression of ectocranial suture fusion among Hominidae (Homo, Pan, Gorilla, and Pongo), Hylobates, and Cercopithecidae (Macaca and Papio) groups. Our hypothesis is that suture fusion patterns should reflect their evolutionary relationship. For the lateral-anterior suture sites there appear to be three major patterns of fusion, one shared by Homo-Pan-Gorilla, anterior to posterior; one shared by Pongo and Hylobates, superior to inferior; and one shared by Cercopithecidae, posterior to anterior. For the vault suture pattern, the Hominidae groups reflect the known phylogeny. The data for Hylobates and Cercopithecidae groups is less clear. The vault suture site termination pattern of Papio is similar to that reported for Gorilla and Pongo. Thus, it may be that some suture sites are under larger genetic influence for patterns of fusion, while others are influenced by environmental/biomechanic influences.

Ecological divergence and talar morphology in gorillas.

Gorillas occupy a variety of habitats from the west coast to eastern central Africa. These habitats differ considerably in altitude, which has a pronounced effect on forest ecology. Although all gorillas are obligate terrestrial knuckle-walking quadrupeds, those that live in lowland habitats eat fruits and climb more often than do those living in highland habitats. Here we test the hypothesis that gorilla talus morphology falls along a morphocline that tracks locomotor function related to a more inverted or everted foot set. This proposed morphocline predicts that gorillas living in lowland habitats may have a talocrural joint configured to facilitate a more medially oriented foot during climbing, suggesting that they may be more adaptively committed to arboreality than gorillas living in highland habitats. To quantify the relative set of the foot in gorillas, we chose two three-dimensional measurements of the talocrural joint: mediolateral curvature of the trochlea and relative surface area of the lateral malleolus. Our results show that, in comparison to their eastern counterparts, western gorillas have talar features that reflect a more medially directed sole of the foot. This morphology likely facilitates foot placement in a wider range of positions and minimization of shearing stresses across the joint when the foot is loaded on more curved or vertically oriented substrates as occurs during climbing and other arboreal behaviors. In contrast, eastern gorilla talar morphology is consistent with habitual placement of the foot with the sole directed more inferiorly, suggesting more effective loading during plantigrade push-off on terrestrial substrates.

Great ape genetic diversity and population history.

Most great ape genetic variation remains uncharacterized; however, its study is critical for understanding population history, recombination, selection and susceptibility to disease. Here we sequence to high coverage a total of 79 wild- and captive-born individuals representing all six great ape species and seven subspecies and report 88.8 million single nucleotide polymorphisms. Our analysis provides support for genetically distinct populations within each species, signals of gene flow, and the split of common chimpanzees into two distinct groups: Nigeria-Cameroon/western and central/eastern populations. We find extensive inbreeding in almost all wild populations, with eastern gorillas being the most extreme. Inferred effective population sizes have varied radically over time in different lineages and this appears to have a profound effect on the genetic diversity at, or close to, genes in almost all species. We discover and assign 1,982 loss-of-function variants throughout the human and great ape lineages, determining that the rate of gene loss has not been different in the human branch compared to other internal branches in the great ape phylogeny. This comprehensive catalogue of great ape genome diversity provides a framework for understanding evolution and a resource for more effective management of wild and captive great ape populations.

Different selective pressures shape the evolution of Toll-like receptors in human and African great ape populations.

The study of the genetic and selective landscape of immunity genes across primates can provide insight into the existing differences in susceptibility to infection observed between human and non-human primates. Here, we explored how selection has driven the evolution of a key family of innate immunity receptors, the Toll-like receptors (TLRs), in African great ape species. We sequenced the 10 TLRs in various populations of chimpanzees and gorillas, and analysed these data jointly with a human data set. We found that purifying selection has been more pervasive in great apes than in humans. Furthermore, in chimpanzees and gorillas, purifying selection has targeted TLRs irrespectively of whether they are endosomal or cell surface, in contrast to humans where strong selective constraints are restricted to endosomal TLRs. These observations suggest important differences in the relative importance of TLR-mediated pathogen sensing, such as that of recognition of flagellated bacteria by TLR5, between humans and great apes. Lastly, we used a population genetics-phylogenetics method that jointly analyses polymorphism and divergence data to detect fine-scale variation in selection pressures at specific codons within TLR genes. We identified different codons at different TLRs as being under positive selection in each species, highlighting that functional variation at these genes has conferred a selective advantage in immunity to infection to specific primate species. Overall, this study showed that the degree of selection driving the evolution of TLRs has largely differed between human and non-human primates, increasing our knowledge on their respective biological contribution to host defence in the natural setting.

Sympatric chimpanzees and gorillas harbor convergent gut microbial communities.

The gut microbial communities within great apes have been shown to reflect the phylogenetic history of their hosts, indicating codiversification between great apes and their gut microbiota over evolutionary timescales. But because the great apes examined to date represent geographically isolated populations whose diets derive from different sources, it is unclear whether this pattern of codiversification has resulted from a long history of coadaptation between microbes and hosts (heritable factors) or from the ecological and geographic separation among host species (environmental factors). To evaluate the relative influences of heritable and environmental factors on the evolution of the great ape gut microbiota, we assayed the gut communities of sympatric and allopatric populations of chimpanzees, bonobos, and gorillas residing throughout equatorial Africa. Comparisons of these populations revealed that the gut communities of different host species can always be distinguished from one another but that the gut communities of sympatric chimpanzees and gorillas have converged in terms of community composition, sharing on average 53% more bacterial phylotypes than the gut communities of allopatric hosts. Host environment, independent of host genetics and evolutionary history, shaped the distribution of bacterial phylotypes across the Bacteroidetes, Firmicutes, Proteobacteria, and Actinobacteria, the four most common phyla of gut bacteria. Moreover, the specific patterns of phylotype sharing among hosts suggest that chimpanzees living in sympatry with gorillas have acquired bacteria from gorillas. These results indicate that geographic isolation between host species has promoted the evolutionary differentiation of great ape gut bacterial communities.