Claudine André

The bonobo genome compared with the chimpanzee and human genomes

Two African apes are the closest living relatives of humans: the chimpanzee (Pan troglodytes) and the bonobo (Pan paniscus). Although they are similar in many respects, bonobos and chimpanzees differ strikingly in key social and sexual behaviours, and for some of these traits they show more similarity with humans than with each other. Here we report the sequencing and assembly of the bonobo genome to study its evolutionary relationship with the chimpanzee and human genomes. We find that more than three per cent of the human genome is more closely related to either the bonobo or the chimpanzee genome than these are to each other. These regions allow various aspects of the ancestry of the two ape species to be reconstructed. In addition, many of the regions that overlap genes may eventually help us understand the genetic basis of phenotypes that humans share with one of the two apes to the exclusion of the other.

Bonobos fall within the genomic variation of chimpanzees

To gain insight into the patterns of genetic variation and evolutionary relationships within and between bonobos and chimpanzees, we sequenced 150,000 base pairs of nuclear DNA divided among 15 autosomal regions as well as the complete mitochondrial genomes from 20 bonobos and 58 chimpanzees. Except for western chimpanzees, we found poor genetic separation of chimpanzees based on sample locality. In contrast, bonobos consistently cluster together but fall as a group within the variation of chimpanzees for many of the regions. Thus, while chimpanzees retain genomic variation that predates bonobo-chimpanzee speciation, extensive lineage sorting has occurred within bonobos such that much of their genome traces its ancestry back to a single common ancestor that postdates their origin as a group separate from chimpanzees.

Comparative Population Genomics of the Ejaculate in Humans and the Great Apes

The rapid molecular evolution of reproductive genes is nearly ubiquitous across animals, yet the selective forces and functional targets underlying this divergence remain poorly understood. Humans and closely related species of great apes show strongly divergent mating systems, providing a powerful system to investigate the influence of sperm competition on the evolution of reproductive genes. This is complemented by detailed information on male reproductive biology and unparalleled genomic resources in humans. Here, we have used custom microarrays to capture and sequence 285 genes encoding proteins present in the ejaculate as well as 101 randomly selected control genes in 21 gorillas, 20 chimpanzees, 20 bonobos, and 20 humans. In total, we have generated >25× average genomic coverage per individual for over 1 million target base pairs. Our analyses indicate high levels of evolutionary constraint across much of the ejaculate combined with more rapid evolution of genes involved in immune defense and proteolysis. We do not find evidence for appreciably more positive selection along the lineage leading to bonobos and chimpanzees, although this would be predicted given more intense sperm competition in these species. Rather, the extent of positive and negative selection depended more on the effective population sizes of the species. Thus, general patterns of male reproductive protein evolution among apes and humans depend strongly on gene function but not on inferred differences in the intensity of sperm competition among extant species.

Long-Term Balancing Selection in LAD1 Maintains a Missense Trans-Species Polymorphism in Humans, Chimpanzees, and Bonobos

Balancing selection maintains advantageous genetic and phenotypic diversity in populations. When selection acts for long evolutionary periods selected polymorphisms may survive species splits and segregate in present-day populations of different species. Here, we investigate the role of long-term balancing selection in the evolution of protein-coding sequences in the Homo-Pan clade. We sequenced the exome of 20 humans, 20 chimpanzees, and 20 bonobos and detected eight coding trans-species polymorphisms (trSNPs) that are shared among the three species and have segregated for approximately 14 My of independent evolution. Although the majority of these trSNPs were found in three genes of the major histocompatibility locus cluster, we also uncovered one coding trSNP (rs12088790) in the gene LAD1. All these trSNPs show clustering of sequences by allele rather than by species and also exhibit other signatures of long-term balancing selection, such as segregating at intermediate frequency and lying in a locus with high genetic diversity. Here, we focus on the trSNP in LAD1, a gene that encodes for Ladinin-1, a collagenous anchoring filament protein of basement membrane that is responsible for maintaining cohesion at the dermal-epidermal junction; the gene is also an autoantigen responsible for linear IgA disease. This trSNP results in a missense change (Leucine257Proline) and, besides altering the protein sequence, is associated with changes in gene expression of LAD1.

The Conservation Value of Lola ya Bonobo Sanctuary

Have you been to a football game lately? Think of the last time you were in an arena that seated fifty or even a hundred thousand people. That many people can make a lot of noise, but of course only represent a tiny piece of humanity today. If we could convince all the bonobos in the world to attend such a game, you could not come close to filling even the smallest professional football stadium. Our closest living relative is slipping off the precipice; their extinction in our own lifetime is a real possibility. The best estimates of the current bonobo population in the wild are somewhere between 5,000–50,000 individuals; all live in the Democratic Republic of Congo (DRC), the only country in which they are found indigenously (Teleki and Baldwin 1979, Kano 1984, Van Krunkelsven 2001). While it might seem an administrative blessing to have bonobos concentrated in one single large country, this rare species still shares all the problems of population fragmentation, habitat loss, and victimization due to the bushmeat trade practice by their African cousins. In addition, by being concentrated in one country, this species’ survival is dependent upon the state of one single nation – for better or worse. The ubiquitous threats to African apes seem particularly acute in the case of the bonobo as a result of DRC’s ill fortune during the past decade. However, the DRC has begun recovering from a decade of wars and now has the chance to jump from an impoverished victim of an oft forgotten war between seven nations, to a regional power as it struggles to redevelop its shattered economy through what to many must seem like an infinite supply of natural resources (Clark 2002). What will the

The saliva microbiome of Pan and Homo

BackgroundIt is increasingly recognized that the bacteria that live in and on the human body (the microbiome) can play an important role in health and disease. The composition of the microbiome is potentially influenced by both internal factors (such as phylogeny and host physiology) and external factors (such as diet and local environment), and interspecific comparisons can aid in understanding the importance of these factors.ResultsTo gain insights into the relative importance of these factors on saliva microbiome diversity, we here analyze the saliva microbiomes of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) from two sanctuaries in Africa, and from human workers at each sanctuary. The saliva microbiomes of the two Pan species are more similar to one another, and the saliva microbiomes of the two human groups are more similar to one another, than are the saliva microbiomes of human workers and apes from the same sanctuary. We also looked for the existence of a core microbiome and find no evidence for a taxon-based core saliva microbiome for Homo or Pan. In addition, we studied the saliva microbiome from apes from the Leipzig Zoo, and found an extraordinary diversity in the zoo ape saliva microbiomes that is not found in the saliva microbiomes of the sanctuary animals.ConclusionsThe greater similarity of the saliva microbiomes of the two Pan species to one another, and of the two human groups to one another, are in accordance with both the phylogenetic relationships of the hosts as well as with host physiology. Moreover, the results from the zoo animals suggest that novel environments can have a large impact on the microbiome, and that microbiome analyses based on captive animals should be viewed with caution as they may not reflect the microbiome of animals in the wild.

Encephalomyocarditis virus mortality in semi‐wild bonobos (Pan panicus)

Background  Fatal myocarditis from encephalomyocarditis virus (EMCV) infection has previously been identified in sporadic and epidemic forms in many species of captive non‐human primates probably including one bonobo (Pan paniscus).

Fatal inflammatory heart disease in a bonobo (Pan paniscus)

Abstract:  We report the first probable identification of encephalomyocarditis virus (EMCV) in a bonobo (Pan paniscus) that had been part of a forest re‐introduction programme. Clinical presentation was of episodic acute on chronic heart failure and cerebral infarction with end‐stage renal failure rather than sudden death which is more commonly associated with EMCV infection. A postmortem diagnosis of probable EMCV was made using gross pathological and histopathological examination. Findings included acute on chronic heart failure combined with the unusual but characteristic histopathological features of non‐suppurative necrotizing myocarditis with mononuclear, inflammatory infiltration of the brain.

Placental retention in a bonobo (Pan paniscus)

Background  This case report describes the first placental retention in an 11‐year‐old female bonobo (Pan paniscus) following the delivery of a healthy infant.

Lineage-Specific Changes in Biomarkers in Great Apes and Humans

Although human biomedical and physiological information is readily available, such information for great apes is limited. We analyzed clinical chemical biomarkers in serum samples from 277 wild- and captive-born great apes and from 312 healthy human volunteers as well as from 20 rhesus macaques. For each individual, we determined a maximum of 33 markers of heart, liver, kidney, thyroid and pancreas function, hemoglobin and lipid metabolism and one marker of inflammation. We identified biomarkers that show differences between humans and the great apes in their average level or activity. Using the rhesus macaques as an outgroup, we identified human-specific differences in the levels of bilirubin, cholinesterase and lactate dehydrogenase, and bonobo-specific differences in the level of apolipoprotein A-I. For the remaining twenty-nine biomarkers there was no evidence for lineage-specific differences. In fact, we find that many biomarkers show differences between individuals of the same species in different environments. Of the four lineage-specific biomarkers, only bilirubin showed no differences between wild- and captive-born great apes. We show that the major factor explaining the human-specific difference in bilirubin levels may be genetic. There are human-specific changes in the sequence of the promoter and the protein-coding sequence of uridine diphosphoglucuronosyltransferase 1 (UGT1A1), the enzyme that transforms bilirubin and toxic plant compounds into water-soluble, excretable metabolites. Experimental evidence that UGT1A1 is down-regulated in the human liver suggests that changes in the promoter may be responsible for the human-specific increase in bilirubin. We speculate that since cooking reduces toxic plant compounds, consumption of cooked foods, which is specific to humans, may have resulted in relaxed constraint on UGT1A1 which has in turn led to higher serum levels of bilirubin in humans.