Christian Roos

Mitogenomics of the Old World monkey tribe Papionini

BackgroundThe evolutionary history of the Old World monkey tribe Papionini comprising the genera Macaca, Mandrillus, Cercocebus, Lophocebus, Theropithecus, Rungwecebus and Papio is still matter of debate. Although the African Papionini (subtribe Papionina) are generally considered to be the sister lineage to the Asian Papionini (subtribe Macacina), previous studies based on morphological data, nuclear or mitochondrial sequences have shown contradictory phylogenetic relationships among and within both subtribes. To further elucidate the phylogenetic relationships among papionins and to estimate divergence ages we generated mitochondrial genome data and combined them with previously published sequences.ResultsOur mitochondrial gene tree comprises 33 papionins representing all genera of the tribe except Rungwecebus. In contrast to most previous studies, the obtained phylogeny suggests a division of the Papionini into three main mitochondrial clades with similar ages: 1) Papio, Theropithecus, Lophocebus; 2) Mandrillus, Cercocebus; and 3) Macaca; the Mandrillus + Cercocebus clade appears to be more closely related to Macaca than to the other African Papionini. Further, we find paraphyletic relationships within the Mandrillus + Cercocebus clade as well as in Papio. Relationships among Theropithecus, Lophocebus and Papio remain unresolved. Divergence ages reveal initial splits within the three mitochondrial clades around the Miocene/Pliocene boundary and differentiation of Macaca species groups occurred on a similar time scale as those found between genera of the subtribe Papionina.ConclusionDue to the largely well-resolved mitochondrial phylogeny, our study provides new insights into the evolutionary history of the Papionini. Results show some contradictory relationships in comparison to previous analyses, notably the paraphyly within the Cercocebus + Mandrillus clade and three instead of only two major mitochondrial clades. Divergence ages among species groups of macaques are similar to those among African Papionini genera, suggesting that diversification of the mitochondrial genome is of a similar magnitude in both subtribes. However, since our mitochondrial tree represents just a single gene tree that most likely does not reflect the true species tree, extensive nuclear sequence data is required to illuminate the true species phylogeny of papionins and to trace possible ancient hybridization events among lineages.

The application of “-omics” technologies for the classification and identification of animals

The correct classification of organisms based on specific rules is essential in biological sciences. Traditionally, morphological characteristics such as size, shape, color, and anatomical structures have been used to identify and classify species. However, as consequence of the tremendous advances in molecular technologies during the last years, new approaches have become available for taxonomic research. Various modern high-throughput technologies allow the detailed characterization of the genome, proteome, metabolome as well as the morphology of an organism. Furthermore, the open access storage of such comprehensive data sets as part of an uprising digital cybertaxonomy enables highly fascinating digital dimensions for modern taxonomy, including the buildup of virtual collections as well as data sets for 3D printing techniques that can be used to replicate complete voucher specimens or at least important diagnostic characters. As a result of these advances, we are now able to document, describe, and identify species much more comprehensively than just a few years ago. In this review we provide an overview about the technical advances in taxonomic research in recent years and discuss their power and limitations.

Pan-African Voyagers: The Phylogeography of Baboons

Baboons of the genus Papio have colonised wide areas of Africa and parts of the Arabian Peninsula. Traditionally, 5 phenotypically distinct morphotypes (species) are recognised: chacma baboons, yellow baboons, olive baboons, Guinea baboons and hamadryas baboons. We used mitochondrial DNA (“Brown” region) sequence data obtained mainly from faecal samples collected across the geographical range of baboons to reconstruct their phylogenetic relationships. Eight well-supported major haplogroups were detected, which reflect geographic populations. These disagree with the traditional classification of baboons into only 5 taxa. We found that West African olive and chacma baboons both comprise at least two deeply separated clades. In the case of chacma baboons, they correspond to recognised morphotypes (Cape chacma and grey-footed chacma). Our data also support a previously suggested distinction between yellow and Kinda baboons from central Zambia. Two other terminal clades from eastern Africa comprise either eastern olive and hamadryas baboons or eastern olive and yellow baboons. Southern yellow baboons cluster with grey-footed chacma baboons. Our data also indicate a possible mitochondrial overlap between Guinea baboons and a particular lineage of western olive baboons from Ivory Coast. These results support recent molecular studies, which detected several para- and polyphyletic mitochondrial clades in Papio, suggesting that the evolutionary history of baboons is even more complicated than previously thought. Thus, important roles might have been played by multiple phases of fragmentation, isolation, hybridisation, introgression, and nuclear swamping, hence, reticulation. These processes were most likely triggered by multiple cycles of expansion and retreat of savannah biomes during late Pliocene and Pleistocene glacial and inter-glacial periods. We also speculate on the likely dispersal pathways of these primates that may have led to their current distribution.

Human-specific CpG “beacons” identify loci associated with human-specific traits and disease

Regulatory change has long been hypothesized to drive the delineation of the human phenotype from other closely related primates. Here we provide evidence that CpG dinucleotides play a special role in this process. CpGs enable epigenome variability via DNA methylation, and this epigenetic mark functions as a regulatory mechanism. Therefore, species-specific CpGs may influence species-specific regulation. We report non-polymorphic species-specific CpG dinucleotides (termed “CpG beacons”) as a distinct genomic feature associated with CpG island (CGI) evolution, human traits and disease. Using an inter-primate comparison, we identified 21 extreme CpG beacon clusters (≥ 20/kb peaks, empirical p < 1.0 × 10−3) in humans, which include associations with four monogenic developmental and neurological disease related genes (Benjamini-Hochberg corrected p = 6.03 × 10−3). We also demonstrate that beacon-mediated CpG density gain in CGIs correlates with reduced methylation in these species in orthologous CGIs over time, via human, chimpanzee and macaque MeDIP-seq. Therefore mapping into both the genomic and epigenomic space the identified CpG beacon clusters define points of intersection where a substantial two-way interaction between genetic sequence and epigenetic state has occurred. Taken together, our data support a model for CpG beacons to contribute to CGI evolution from genesis to tissue-specific to constitutively active CGIs.

Species definitions and conservation: a review and case studies from African mammals

The nature of species, especially as applied to large mammals, is of major concern in conservation. Here, we briefly comment on recent thinking in alpha taxonomy, and assert that species are in essence evolutionary lineages, and that the most effective way of recognising them is by their diagnosability, i.e. the so-called Phylogenetic Species Concept. We further assert that the amount of genetic distance is not a relevant datum for distinguishing species, and that the ability to interbreed is not relevant. We consider a few case studies, especially that of the Northern White Rhinoceros Ceratotherium cottoni, and also species in Loxodonta, Giraffa and Oreotragus.

Human-specific epigenetic variation in the immunological Leukotriene B4 Receptor (LTB4R/BLT1) implicated in common inflammatory diseases

BackgroundCommon human diseases are caused by the complex interplay of genetic susceptibility as well as environmental factors. Due to the environment’s influence on the epigenome, and therefore genome function, as well as conversely the genome’s facilitative effect on the epigenome, analysis of this level of regulation may increase our knowledge of disease pathogenesis.MethodsIn order to identify human-specific epigenetic influences, we have performed a novel genome-wide DNA methylation analysis comparing human, chimpanzee and rhesus macaque.ResultsWe have identified that the immunological Leukotriene B4 receptor (LTB4R, BLT1 receptor) is the most epigenetically divergent human gene in peripheral blood in comparison with other primates. This difference is due to the co-ordinated active state of human-specific hypomethylation in the promoter and human-specific increased gene body methylation. This gene is significant in innate immunity and the LTB4/LTB4R pathway is involved in the pathogenesis of the spectrum of human inflammatory diseases. This finding was confirmed by additional neutrophil-only DNA methylome and lymphoblastoid H3K4me3 chromatin comparative data. Additionally we show through functional analysis that this receptor has increased expression and a higher response to the LTB4 ligand in human versus rhesus macaque peripheral blood mononuclear cells. Genome-wide we also find human species-specific differentially methylated regions (human s-DMRs) are more prevalent in CpG island shores than within the islands themselves, and within the latter are associated with the CTCF motif.ConclusionsThis result further emphasises the exclusive nature of the human immunological system, its divergent adaptation even from very closely related primates, and the power of comparative epigenomics to identify and understand human uniqueness.

Discordance Between Spatial Distributions of Y-Chromosomal and Mitochondrial Haplotypes in African Green Monkeys (Chlorocebus spp.): A Result of Introgressive Hybridization or Cryptic Diversity?

Introgressive hybridization may cause substantial discordances among phylogenies based on different genetic markers. Such discordances have been found in diverse mammal species including primates. A recent study of mitochondrial DNA (mtDNA) revealed several poly- and paraphyletic relationships in African green monkeys (Chlorocebus), suggesting contemporary and/or ancient introgressive hybridization among almost all parapatric species of the genus. However, mtDNA analyses alone do not allow us to draw conclusions concerning introgression events. In this study we analyzed two Y chromosomal (Y-chr) markers for 30 African green monkey samples and compared the resulting genetic relationships to those based on published mtDNA data. In line with the results for mtDNA, we found no Y-chr evidence of hypothesized hybridization among Chlorocebus sabaeus and C. tantalus in the northern part of the contact zone in West Africa, and we found two distinct and distantly related Y-chr haplotypes within the range of C. tantalus, suggesting possible cryptic genetic diversity rather than ancient introgressive hybridization in this species. In contrast, Y-chr data revealed monophyletic relationships within Chlorocebus pygerythrus from East Africa, suggesting that mtDNA paraphylies found in this species are most likely to be the result of ancient introgressive hybridization and subsequent cytonuclear extinction of an earlier taxon. Our results accentuate the importance of analyzing sex chromosomal data in addition to mtDNA to obtain more information on the potential outcomes of hybridization with respect to genetic and species diversity. Analysis of more diverse nuclear marker sets is needed to obtain a more complete picture of the African green monkey evolution.

Differentiated adaptive evolution, episodic relaxation of selective constraints, and pseudogenization of umami and sweet taste genes TAS1Rs in catarrhine primates

BackgroundUmami and sweet tastes are two important basic taste perceptions that allow animals to recognize diets with nutritious carbohydrates and proteins, respectively. Until recently, analyses of umami and sweet taste were performed on various domestic and wild animals. While most of these studies focused on the pseudogenization of taste genes, which occur mostly in carnivores and species with absolute feeding specialization, omnivores and herbivores were more or less neglected. Catarrhine primates are a group of herbivorous animals (feeding mostly on plants) with significant divergence in dietary preference, especially the specialized folivorous Colobinae. Here, we conducted the most comprehensive investigation to date of selection pressure on sweet and umami taste genes (TAS1Rs) in catarrhine primates to test whether specific adaptive evolution occurred during their diversification, in association with particular plant diets.ResultsWe documented significant relaxation of selective constraints on sweet taste gene TAS1R2 in the ancestral branch of Colobinae, which might correlate with their unique ingestion and digestion of leaves. Additionally, we identified positive selection acting on Cercopithecidae lineages for the umami taste gene TAS1R1, on the Cercopithecinae and extant Colobinae and Hylobatidae lineages for TAS1R2, and on Macaca lineages for TAS1R3. Our research further identified several site mutations in Cercopithecidae, Colobinae and Pygathrix, which were detected by previous studies altering the sensitivity of receptors. The positively selected sites were located mostly on the extra-cellular region of TAS1Rs. Among these positively selected sites, two vital sites for TAS1R1 and four vital sites for TAS1R2 in extra-cellular region were identified as being responsible for the binding of certain sweet and umami taste molecules through molecular modelling and docking.ConclusionsOur results suggest that episodic and differentiated adaptive evolution of TAS1Rs pervasively occurred in catarrhine primates, most concentrated upon the extra-cellular region of TAS1Rs.

Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation

Primates occur in 90 countries, but four—Brazil, Madagascar, Indonesia, and the Democratic Republic of the Congo (DRC)—harbor 65% of the world’s primate species (439) and 60% of these primates are Threatened, Endangered, or Critically Endangered (IUCN Red List of Threatened Species 2017-3). Considering their importance for global primate conservation, we examine the anthropogenic pressures each country is facing that place their primate populations at risk. Habitat loss and fragmentation are main threats to primates in Brazil, Madagascar, and Indonesia. However, in DRC hunting for the commercial bushmeat trade is the primary threat. Encroachment on primate habitats driven by local and global market demands for food and non-food commodities hunting, illegal trade, the proliferation of invasive species, and human and domestic-animal borne infectious diseases cause habitat loss, population declines, and extirpation. Modeling agricultural expansion in the 21st century for the four countries under a worst-case-scenario, showed a primate range contraction of 78% for Brazil, 72% for Indonesia, 62% for Madagascar, and 32% for DRC. These pressures unfold in the context of expanding human populations with low levels of development. Weak governance across these four countries may limit effective primate conservation planning. We examine landscape and local approaches to effective primate conservation policies and assess the distribution of protected areas and primates in each country. Primates in Brazil and Madagascar have 38% of their range inside protected areas, 17% in Indonesia and 14% in DRC, suggesting that the great majority of primate populations remain vulnerable. We list the key challenges faced by the four countries to avert primate extinctions now and in the future. In the short term, effective law enforcement to stop illegal hunting and illegal forest destruction is absolutely key. Long-term success can only be achieved by focusing local and global public awareness, and actively engaging with international organizations, multinational businesses and consumer nations to reduce unsustainable demands on the environment. Finally, the four primate range countries need to ensure that integrated, sustainable land-use planning for economic development includes the maintenance of biodiversity and intact, functional natural ecosystems.