Primate Phylogeny and Genetics

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Population and Evolutionary Genetics and Genomics".

Deadline for manuscript submissions: closed (31 December 2022) | Viewed by 34076

Special Issue Editors


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Guest Editor
Institute of Zoology, University of Veterinary Medicine Hannover, 30559 Hannover, Germany
Interests: evolution; conservation genetics; behavioral ecology; lemurs; primates; biodiversity

E-Mail Website
Guest Editor
Gene Bank of Primates and Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, 37077 Goettingen, Germany
Interests: evolution; phylogeny; genomics; conservation genetics; colobines; gibbons; primates; biodiversity

Special Issue Information

Dear Colleagues,

New phylogenetic tools and population genetics methods have been developed and vastly advanced over the last decade. For example, they allow to better delimitate cryptic species, infer species trees under incomplete lineage sorting, model alternative demographic population histories, investigate phenotype–genotype interactions, or infer barriers to gene flow in various types of landscape. Non-human primates comprise more than 500 species worldwide, with the majority of them (66.6%) being listed as threatened by the IUCN (www.redlist.org). For many of them, detailed genetic studies on their population structure and the effects of habitat fragmentation on genetic diversity, local adaptation, phylogeographic history, or on their exact phylogenetic position are still missing.

We encourage submissions of unpublished original manuscripts (research articles, reviews, and communications) on non-human primates with a strong genetic or genomic component describing recent advances on all aspects related, but not limited to, the following topics: phylogenetic inference, population genetics, genetic diversity, local adaptation, genetic structure, phylogeographic inference, demographic modeling, landscape genetics, and hybridization.

Prof. Dr. Ute Radespiel
Prof. Dr. Christian Roos
Guest Editors

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Keywords

  • phylogenetic inference
  • population genetics
  • phylogeography
  • demographic modeling
  • landscape genetics
  • genomics
  • hybridization
  • local adaptation

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Published Papers (11 papers)

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Research

Jump to: Review

16 pages, 896 KiB  
Article
Whole Genome Analysis of SNV and Indel Polymorphism in Common Marmosets (Callithrix jacchus)
by R. Alan Harris, Muthuswamy Raveendran, Wes Warren, Hillier W. LaDeana, Chad Tomlinson, Tina Graves-Lindsay, Richard E. Green, Jenna K. Schmidt, Julia C. Colwell, Allison T. Makulec, Shelley A. Cole, Ian H. Cheeseman, Corinna N. Ross, Saverio Capuano III, Evan E. Eichler, Jon E. Levine and Jeffrey Rogers
Genes 2023, 14(12), 2185; https://doi.org/10.3390/genes14122185 - 7 Dec 2023
Cited by 1 | Viewed by 2341
Abstract
The common marmoset (Callithrix jacchus) is one of the most widely used nonhuman primate models of human disease. Owing to limitations in sequencing technology, early genome assemblies of this species using short-read sequencing suffered from gaps. In addition, the genetic diversity [...] Read more.
The common marmoset (Callithrix jacchus) is one of the most widely used nonhuman primate models of human disease. Owing to limitations in sequencing technology, early genome assemblies of this species using short-read sequencing suffered from gaps. In addition, the genetic diversity of the species has not yet been adequately explored. Using long-read genome sequencing and expert annotation, we generated a high-quality genome resource creating a 2.898 Gb marmoset genome in which most of the euchromatin portion is assembled contiguously (contig N50 = 25.23 Mbp, scaffold N50 = 98.2 Mbp). We then performed whole genome sequencing on 84 marmosets sampling the genetic diversity from several marmoset research centers. We identified a total of 19.1 million single nucleotide variants (SNVs), of which 11.9 million can be reliably mapped to orthologous locations in the human genome. We also observed 2.8 million small insertion/deletion variants. This dataset includes an average of 5.4 million SNVs per marmoset individual and a total of 74,088 missense variants in protein-coding genes. Of the 4956 variants orthologous to human ClinVar SNVs (present in the same annotated gene and with the same functional consequence in marmoset and human), 27 have a clinical significance of pathogenic and/or likely pathogenic. This important marmoset genomic resource will help guide genetic analyses of natural variation, the discovery of spontaneous functional variation relevant to human disease models, and the development of genetically engineered marmoset disease models. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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12 pages, 2016 KiB  
Article
A Pervasive History of Gene Flow in Madagascar’s True Lemurs (Genus Eulemur)
by Kathryn M. Everson, Mariah E. Donohue and David W. Weisrock
Genes 2023, 14(6), 1130; https://doi.org/10.3390/genes14061130 - 23 May 2023
Viewed by 1775
Abstract
In recent years, it has become widely accepted that interspecific gene flow is common across the Tree of Life. Questions remain about how species boundaries can be maintained in the face of high levels of gene flow and how phylogeneticists should account for [...] Read more.
In recent years, it has become widely accepted that interspecific gene flow is common across the Tree of Life. Questions remain about how species boundaries can be maintained in the face of high levels of gene flow and how phylogeneticists should account for reticulation in their analyses. The true lemurs of Madagascar (genus Eulemur, 12 species) provide a unique opportunity to explore these questions, as they form a recent radiation with at least five active hybrid zones. Here, we present new analyses of a mitochondrial dataset with hundreds of individuals in the genus Eulemur, as well as a nuclear dataset containing hundreds of genetic loci for a small number of individuals. Traditional coalescent-based phylogenetic analyses of both datasets reveal that not all recognized species are monophyletic. Using network-based approaches, we also find that a species tree containing between one and three ancient reticulations is supported by strong evidence. Together, these results suggest that hybridization has been a prominent feature of the genus Eulemur in both the past and present. We also recommend that greater taxonomic attention should be paid to this group so that geographic boundaries and conservation priorities can be better established. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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23 pages, 3380 KiB  
Article
A New Assessment of Robust Capuchin Monkey (Sapajus) Evolutionary History Using Genome-Wide SNP Marker Data and a Bayesian Approach to Species Delimitation
by Amely Branquinho Martins, Mônica Mafra Valença-Montenegro, Marcela Guimarães Moreira Lima, Jessica W. Lynch, Walfrido Kühl Svoboda, José de Sousa e Silva-Júnior, Fábio Röhe, Jean Philippe Boubli and Anthony Di Fiore
Genes 2023, 14(5), 970; https://doi.org/10.3390/genes14050970 - 25 Apr 2023
Cited by 5 | Viewed by 2566
Abstract
Robust capuchin monkeys, Sapajus genus, are among the most phenotypically diverse and widespread groups of primates in South America, with one of the most confusing and often shifting taxonomies. We used a ddRADseq approach to generate genome-wide SNP markers for 171 individuals from [...] Read more.
Robust capuchin monkeys, Sapajus genus, are among the most phenotypically diverse and widespread groups of primates in South America, with one of the most confusing and often shifting taxonomies. We used a ddRADseq approach to generate genome-wide SNP markers for 171 individuals from all putative extant species of Sapajus to access their evolutionary history. Using maximum likelihood, multispecies coalescent phylogenetic inference, and a Bayes Factor method to test for alternative hypotheses of species delimitation, we inferred the phylogenetic history of the Sapajus radiation, evaluating the number of discrete species supported. Our results support the recognition of three species from the Atlantic Forest south of the São Francisco River, with these species being the first splits in the robust capuchin radiation. Our results were congruent in recovering the Pantanal and Amazonian Sapajus as structured into three monophyletic clades, though new morphological assessments are necessary, as the Amazonian clades do not agree with previous morphology-based taxonomic distributions. Phylogenetic reconstructions for Sapajus occurring in the Cerrado, Caatinga, and northeastern Atlantic Forest were less congruent with morphology-based phylogenetic reconstructions, as the bearded capuchin was recovered as a paraphyletic clade, with samples from the Caatinga biome being either a monophyletic clade or nested with the blond capuchin monkey. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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25 pages, 9121 KiB  
Article
Terrain Ruggedness and Canopy Height Predict Short-Range Dispersal in the Critically Endangered Black-and-White Ruffed Lemur
by Amanda N. Mancini, Aparna Chandrashekar, Jean Pierre Lahitsara, Daisy Gold Ogbeta, Jeanne Arline Rajaonarivelo, Ndimbintsoa Rojoarinjaka Ranaivorazo, Joseane Rasoazanakolona, Mayar Safwat, Justin Solo, Jean Guy Razafindraibe, Georges Razafindrakoto and Andrea L. Baden
Genes 2023, 14(3), 746; https://doi.org/10.3390/genes14030746 - 18 Mar 2023
Viewed by 3176
Abstract
Dispersal is a fundamental aspect of primates’ lives and influences both population and community structuring, as well as species evolution. Primates disperse within an environmental context, where both local and intervening environmental factors affect all phases of dispersal. To date, research has primarily [...] Read more.
Dispersal is a fundamental aspect of primates’ lives and influences both population and community structuring, as well as species evolution. Primates disperse within an environmental context, where both local and intervening environmental factors affect all phases of dispersal. To date, research has primarily focused on how the intervening landscape influences primate dispersal, with few assessing the effects of local habitat characteristics. Here, we use a landscape genetics approach to examine between- and within-site environmental drivers of short-range black-and-white ruffed lemur (Varecia variegata) dispersal in the Ranomafana region of southeastern Madagascar. We identified the most influential drivers of short-range ruffed lemur dispersal as being between-site terrain ruggedness and canopy height, more so than any within-site habitat characteristic evaluated. Our results suggest that ruffed lemurs disperse through the least rugged terrain that enables them to remain within their preferred tall-canopied forest habitat. Furthermore, we noted a scale-dependent environmental effect when comparing our results to earlier landscape characteristics identified as driving long-range ruffed lemur dispersal. We found that forest structure drives short-range dispersal events, whereas forest presence facilitates long-range dispersal and multigenerational gene flow. Together, our findings highlight the importance of retaining high-quality forests and forest continuity to facilitate dispersal and maintain functional connectivity in ruffed lemurs. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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15 pages, 1817 KiB  
Article
Past Connectivity but Recent Inbreeding in Cross River Gorillas Determined Using Whole Genomes from Single Hairs
by Marina Alvarez-Estape, Harvinder Pawar, Claudia Fontsere, Amber E. Trujillo, Jessica L. Gunson, Richard A. Bergl, Magdalena Bermejo, Joshua M. Linder, Kelley McFarland, John F. Oates, Jacqueline L. Sunderland-Groves, Joseph Orkin, James P. Higham, Karine A. Viaud-Martinez, Esther Lizano and Tomas Marques-Bonet
Genes 2023, 14(3), 743; https://doi.org/10.3390/genes14030743 - 18 Mar 2023
Cited by 3 | Viewed by 4424
Abstract
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 [...] Read more.
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. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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0 pages, 4147 KiB  
Article
Molecular Phylogenetic Relationships and Unveiling Novel Genetic Diversity among Slow and Pygmy Lorises, including Resurrection of Xanthonycticebus intermedius
by Mary E. Blair, Giang T. H. Cao, Elora H. López-Nandam, Daniel A. Veronese-Paniagua, Mark G. Birchette, Marina Kenyon, Badrul M. Md-Zain, Rachel A. Munds, K. Anne-Isola Nekaris, Vincent Nijman, Christian Roos, Hoàng M. Thach, Eleanor J. Sterling and Minh D. Le
Genes 2023, 14(3), 643; https://doi.org/10.3390/genes14030643 - 3 Mar 2023
Cited by 8 | Viewed by 5327 | Correction
Abstract
Genetic analysis of historical museum collections presents an opportunity to clarify the evolutionary history of understudied primate groups, improve taxonomic inferences, and inform conservation efforts. Among the most understudied primate groups, slow and pygmy lorises (genera Nycticebus and Xanthonycticebus) are nocturnal strepsirrhines [...] Read more.
Genetic analysis of historical museum collections presents an opportunity to clarify the evolutionary history of understudied primate groups, improve taxonomic inferences, and inform conservation efforts. Among the most understudied primate groups, slow and pygmy lorises (genera Nycticebus and Xanthonycticebus) are nocturnal strepsirrhines found in South and Southeast Asia. Previous molecular studies have supported five species, but studies using morphological data suggest the existence of at least nine species. We sequenced four mitochondrial loci, CO1, cytb, d-loop, and ND4, for a total of 3324 aligned characters per sample from 41 historical museum specimens for the most comprehensive geographic coverage to date for these genera. We then combined these sequences with a larger dataset composed of samples collected in Vietnam as well as previously published sequences (total sample size N = 62). We inferred phylogenetic relationships using Bayesian inference and maximum likelihood methods based on data from each locus and on concatenated sequences. We also inferred divergence dates for the most recent common ancestors of major lineages using a BEAST analysis. Consistent with previous studies, we found support for Xanthonycticebus pygmaeus as a basal taxon to the others in the group. We also confirmed the separation between lineages of X. pygmaeus from northern Vietnam/Laos/China and southern Vietnam/Cambodia and included a taxonomic revision recognizing a second taxon of pygmy loris, X. intermedius. Our results found support for multiple reciprocally monophyletic taxa within Borneo and possibly Java. The study will help inform conservation management of these trade-targeted animals as part of a genetic reference database for determining the taxonomic unit and provenance of slow and pygmy lorises confiscated from illegal wildlife trade activities. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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14 pages, 3116 KiB  
Article
Metatranscriptomic Analyses Reveal Important Roles of the Gut Microbiome in Primate Dietary Adaptation
by Mingyi Zhang, Xiaochen Wang, Ziming Wang, Shuxin Mao, Jiali Zhang, Ming Li and Huijuan Pan
Genes 2023, 14(1), 228; https://doi.org/10.3390/genes14010228 - 15 Jan 2023
Cited by 8 | Viewed by 2952
Abstract
The gut microbiome plays a vital role in host ecological adaptation, especially dietary adaptations. Primates have evolved a variety of dietary and gut physiological structures that are useful to explore the role of the gut microbiome in host dietary adaptations. Here, we characterize [...] Read more.
The gut microbiome plays a vital role in host ecological adaptation, especially dietary adaptations. Primates have evolved a variety of dietary and gut physiological structures that are useful to explore the role of the gut microbiome in host dietary adaptations. Here, we characterize gut microbiome transcriptional activity in ten fecal samples from primates with three different diets and compare the results to their previously reported metagenomic profile. Bacteria related to cellulose degradation, like Bacteroidaceae and Alcaligenaceae, were enriched and actively expressed in the gut microbiome of folivorous primates, and functional analysis revealed that the glycan biosynthesis and metabolic pathways were significantly active. In omnivorous primates, Helicobacteraceae, which promote lipid metabolism, were significantly enriched in expression, and activity and xenobiotic biodegradation and metabolism as well as lipid metabolism pathways were significantly active. In frugivorous primates, the abundance and activity of Elusimicrobiaceae, Neisseriaceae, and Succinivibrionaceae, which are associated with digestion of pectin and fructose, were significantly elevated, and the functional pathways involved in the endocrine system were significantly enriched. In conclusion, the gut microbiome contributes to host dietary adaptation by helping hosts digest the inaccessible nutrients in their specific diets. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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15 pages, 1921 KiB  
Article
Owl Monkey Alu Insertion Polymorphisms and Aotus Phylogenetics
by Jessica M. Storer, Jerilyn A. Walker, Lydia C. Rewerts, Morgan A. Brown, Thomas O. Beckstrom, Scott W. Herke, Christian Roos and Mark A. Batzer
Genes 2022, 13(11), 2069; https://doi.org/10.3390/genes13112069 - 8 Nov 2022
Cited by 2 | Viewed by 1976
Abstract
Owl monkeys (genus Aotus), or “night monkeys” are platyrrhine primates in the Aotidae family. Early taxonomy only recognized one species, Aotus trivirgatus, until 1983, when Hershkovitz proposed nine unique species designations, classified into red-necked and gray-necked species groups based predominately on [...] Read more.
Owl monkeys (genus Aotus), or “night monkeys” are platyrrhine primates in the Aotidae family. Early taxonomy only recognized one species, Aotus trivirgatus, until 1983, when Hershkovitz proposed nine unique species designations, classified into red-necked and gray-necked species groups based predominately on pelage coloration. Recent studies questioned this conventional separation of the genus and proposed designations based on the geographical location of wild populations. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. A scaffold-level genome assembly for one Aotus species, Aotus nancymaae [Anan_2.0], facilitated large-scale ascertainment of nearly 2000 young lineage-specific Alu insertions. This study provides candidate oligonucleotides for locus-specific PCR assays for over 1350 of these elements. For 314 Alu elements across four taxa with multiple specimens, PCR analyses identified 159 insertion polymorphisms, including 21 grouping A. nancymaae and Aotus azarae (red-necked species) as sister taxa, with Aotus vociferans and A. trivirgatus (gray-necked) being more basal. DNA sequencing identified five novel Alu elements from three different taxa. The Alu datasets reported in this study will assist in species identification and provide a valuable resource for Aotus phylogenetics, population genetics and conservation strategies when applied to wild populations. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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22 pages, 2974 KiB  
Article
Nuclear and Mitochondrial Phylogenomics of the Sifakas Reveal Cryptic Variation in the Diademed Sifaka
by Melissa T. R. Hawkins, Carolyn A. Bailey, Allyshia M. Brown, Jen Tinsman, Ryan A. Hagenson, Ryan R. Culligan, Adena G. Barela, Jean C. Randriamanana, Jean F. Ranaivoarisoa, John R. Zaonarivelo and Edward E. Louis, Jr.
Genes 2022, 13(6), 1026; https://doi.org/10.3390/genes13061026 - 7 Jun 2022
Cited by 2 | Viewed by 2745
Abstract
The most comprehensive phylogenomic reconstruction to date was generated on all nominal taxa within the lemur genus Propithecus. Over 200 wild-caught individuals were included in this study to evaluate the intra and interspecific relationships across this genus. Ultraconserved Elements (UCEs) resulted in [...] Read more.
The most comprehensive phylogenomic reconstruction to date was generated on all nominal taxa within the lemur genus Propithecus. Over 200 wild-caught individuals were included in this study to evaluate the intra and interspecific relationships across this genus. Ultraconserved Elements (UCEs) resulted in well-supported phylogenomic trees. Complete mitochondrial genomes (CMGs) largely agreed with the UCEs, except where a mitochondrial introgression was detected between one clade of the diademed sifaka (Propithecus diadema) and the Milne-Edwards sifaka (P. edwardsi). Additionally, the crowned (P. coronatus) and Von der Decken’s (P. deckeni) sifakas belonged to a single admixed lineage from UCEs. Further sampling across these two species is warranted to determine if our sampling represents a hybrid zone. P. diadema recovered two well-supported clades, which were dated and estimated as being ancient as the split between the Perrier’s (P. perrierii) and silky (P. candidus) sifakas. The reconstructed demographic history of the two clades also varied over time. We then modeled the modern ecological niches of the two cryptic P. diadema clades and found that they were significantly diverged (p < 0.01). These ecological differences result in a very limited zone of geographic overlap for the P. diadema clades (<60 km2). Niche models also revealed that the Onive River acts as a potential barrier to dispersal between P. diadema and P. edwardsi. Further taxonomic work is required on P. diadema to determine if its taxonomic status should be revised. This first genomic evaluation of the genus resolved the relationships between the taxa and the recovered cryptic diversity within one species. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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Review

Jump to: Research

15 pages, 2205 KiB  
Review
Recent Advances in Genetics and Genomics of Snub-Nosed Monkeys (Rhinopithecus) and Their Implications for Phylogeny, Conservation, and Adaptation
by Weimin Kuang, Dietmar Zinner, Yuan Li, Xueqin Yao, Christian Roos and Li Yu
Genes 2023, 14(5), 985; https://doi.org/10.3390/genes14050985 - 27 Apr 2023
Cited by 3 | Viewed by 2723
Abstract
The snub-nosed monkey genus Rhinopithecus (Colobinae) comprises five species (Rhinopithecus roxellana, Rhinopithecus brelichi, Rhinopithecus bieti, Rhinopithecus strykeri, and Rhinopithecus avunculus). They are range-restricted species occurring only in small areas in China, Vietnam, and Myanmar. All extant species [...] Read more.
The snub-nosed monkey genus Rhinopithecus (Colobinae) comprises five species (Rhinopithecus roxellana, Rhinopithecus brelichi, Rhinopithecus bieti, Rhinopithecus strykeri, and Rhinopithecus avunculus). They are range-restricted species occurring only in small areas in China, Vietnam, and Myanmar. All extant species are listed as endangered or critically endangered by the International Union for Conservation of Nature (IUCN) Red List, all with decreasing populations. With the development of molecular genetics and the improvement and cost reduction in whole-genome sequencing, knowledge about evolutionary processes has improved largely in recent years. Here, we review recent major advances in snub-nosed monkey genetics and genomics and their impact on our understanding of the phylogeny, phylogeography, population genetic structure, landscape genetics, demographic history, and molecular mechanisms of adaptation to folivory and high altitudes in this primate genus. We further discuss future directions in this research field, in particular how genomic information can contribute to the conservation of snub-nosed monkeys. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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12 pages, 1536 KiB  
Review
A Comprehensive Overview of Baboon Phylogenetic History
by Gisela H. Kopp, Riashna Sithaldeen, Franziska Trede, Franziska Grathwol, Christian Roos and Dietmar Zinner
Genes 2023, 14(3), 614; https://doi.org/10.3390/genes14030614 - 28 Feb 2023
Cited by 2 | Viewed by 2605
Abstract
Baboons (genus Papio) are an intriguing study system to investigate complex evolutionary processes and the evolution of social systems. An increasing number of studies over the last 20 years has shown that considerable incongruences exist between phylogenies based on morphology, mitochondrial, and [...] Read more.
Baboons (genus Papio) are an intriguing study system to investigate complex evolutionary processes and the evolution of social systems. An increasing number of studies over the last 20 years has shown that considerable incongruences exist between phylogenies based on morphology, mitochondrial, and nuclear sequence data of modern baboons, and hybridization and introgression have been suggested as the main drivers of these patterns. Baboons, therefore, present an excellent opportunity to study these phenomena and their impact on speciation. Advances both in geographic and genomic coverage provide increasing details on the complexity of the phylogeography of baboons. Here, we compile the georeferenced genetic data of baboons and review the current knowledge on baboon phylogeny, discuss the evolutionary processes that may have shaped the patterns that we observe today, and propose future avenues for research. Full article
(This article belongs to the Special Issue Primate Phylogeny and Genetics)
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