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An Alu-Based Phylogeny of Gibbons (Hylobatidae)
Abstract and Figures
Gibbons (Hylobatidae) are small, arboreal apes indigenous to Southeast Asia that diverged from other apes ∼15-18 Ma. Extant lineages radiated rapidly 6-10 Ma and are organized into four genera (Hylobates, Hoolock, Symphalangus, and Nomascus) consisting of 12-19 species. The use of short interspersed elements (SINEs) as phylogenetic markers has seen recent popularity due to several desirable characteristics: the ancestral state of a locus is known to be the absence of an element, rare potentially homoplasious events are relatively easy to resolve, and samples can be quickly and inexpensively genotyped. During radiation of primates, one particular family of SINEs, the Alu family, has proliferated in primate genomes. Nomascus leucogenys (northern white-cheeked gibbon) sequences were analyzed for repetitive content with RepeatMasker using a custom library. The sequences containing Alu elements identified as members of a gibbon-specific subfamily were then compared with orthologous positions in other primate genomes. A primate phylogenetic panel consisting of 18 primate species, including 13 gibbon species representing all four extant genera, was assayed for all loci, and a total of 125 gibbon-specific Alu insertions were identified. The resulting amplification patterns were used to generate a phylogenetic tree. We demonstrate significant support for Symphalangus as the most basal lineage within the family. Our findings also place Nomascus as a derived lineage, sister to Hoolock, with the Nomascus-Hoolock clade sister to Hylobates. Further, our analysis groups N. leucogenys and Nomascus siki as sister taxa to the exclusion of the other Nomascus species assayed. This study represents the first use of SINEs to determine the genus level phylogenetic relationships within the family Hylobatidae. These relationships have been resolved with robust support at most internal nodes, demonstrating the utility of SINE-based phylogenetic analysis. We postulate that hybridization and rapid radiation may have contributed to the complex and contradictory findings of the previous studies. Our findings will aid in the conservation of these threatened primates and inform future studies of the biogeographical history and distribution of modern gibbon species.
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... Whole genome sequencing has indicated that the four genera diverged at approximately the same time, perhaps as recently as <5MYA (Veeramah et al., 2015). A combination of rapid speciation and hybridisation/introgression may be responsible for the difficulty of resolving the gibbon phylogeny, and the contradictory results of different studies (Meyer et al., 2012). Furthermore, this historical hybridisation may also be the cause of the massive genome reshuffling observed between the gibbon genera. ...
... For evolutionary studies retrotransposons have a particular advantage over sequence variation, which is that the ancestral state of a locus is always known i.e. absence of the insertion, while DNA substitutions can reverse, falsely indicating homoplasy (Takahashi et al., 2001;Hedges and Batzer, 2005;Kriegs et al., 2006;Frankham, Ballou and Briscoe, 2010;Meyer et al., 2012). Furthermore, genomic removal of ...
... retrotransposons in primates appears unlikely (Hedges and Batzer, 2005). If a retrotransposon is still active during speciation processes, new insertions can occur after the splitting of lineages, and thus be present in one lineage and not another, allowing the two lineages to be distinguished on the basis of presence/absence (see Figure 1.12), while the presence of an insertion in two or more purported species is indicative of sharing a common ancestor (Meyer et al., 2012). Figure 1.12: Transposition events during speciation. ...
... An Alu-based phylogeny of gibbons by Meyer et al. (2012) [21] demonstrate significant support for Symphalangus as the most basal lineage within the family. Their findings also place Nomascus as a derived lineage, sister to Hoolock, with the Nomascus-Hoolock clade sister to Hylobates. ...
... An Alu-based phylogeny of gibbons by Meyer et al. (2012) [21] demonstrate significant support for Symphalangus as the most basal lineage within the family. Their findings also place Nomascus as a derived lineage, sister to Hoolock, with the Nomascus-Hoolock clade sister to Hylobates. ...
Gibbons are a family (Hylobatidae) of ape species endemic to the rainforests of the mainland and islands of Southeast Asia, including four well-recognized genera (Hylobates, Nomascus, Symphalangus, and Hoolock). Most gibbon species are known as considered “endangered” or “critically endangered” (IUCN 2009). This present article gives a review on the research progress of phylogenetic relationships between gibbon species and closely related genera utilizing a range of different traits (e.g., vocalization, morphology, karyotype, mtDNA, Y chromosomes, Autosomes, Alu, and whole genome). Our aim held great potential to clarify more directions in researches on identification of genetic relationship, to provide reference for molecular biology research and useful information for further gibbon research.
... The phylogeny of gibbons has long been a matter of disagreement (Roos and Zinner 2017). Various attempts have been made to reconstruct their evolutionary history through chromosomal karyotypes (Müller et al. 2003), mitochondrial control region (Roos and Geissmann 2001), ND3-ND4 genes (Takacs et al. 2005), nuclear genome elements (Kim et al. 2011), and Alu elements (Meyer et al. 2012). With the advent of newer methods of nucleotide sequencing, whole mitochondrial sequences are available for many species (Chan et al. 2010;Fan et al. 2017;Matsudaira and Ishida 2010). ...
... The confounding of the three genera might be due to the short branch length, suggesting a very short time period between the ancestral Hylobatid and the ancestor of all three genera Hoolock, Hylobates, and Symphalangus. A limited number of nucleotide substitutions may not be enough to provide a well resolved split between these three genera (Matsudaira and Ishida 2010;Meyer et al. 2012;Thinh et al. 2010 Understanding of genetic structure and variation is important for the scientific management and the eventual recovery of endangered species. It was hence imperative to look for genetic evidence as a basis for formulating and implementing conservation management practices for the Hoolock hoolock population. ...
Information about the taxonomy and geographical distribution of a species is essential to understand its evolution and for conservation efforts. The phylogeny of the Hylobatidae remains unclear. India is reported to have one species of Hoolock gibbon (Hoolock hoolock) but a recent study based on pelage colour suggested that another species, H. leuconedys, occurs in the Mishmi Hills between the Dibang and Nao Dehing rivers in Arunachal Pradesh. We examined whether H. leuconedys occurs in India and its evolutionary relationships with other Hylobatidae species. We collected blood, tissue, and fecal samples from various populations of H. hoolock (N = 17) and the Mishmi Hills gibbons (N = 14) from their distribution in Northeast India, zoos, and rescues centers. We isolated DNA from these samples and constructed phylogenetic trees using partial D-loop and COI markers. We also performed whole mitochondrial analysis to study the phylogenetics of the Hylobatidae family. Our genetic analysis showed that none of the samples from India were H. leuconedys, and that all samples from the Mishmi Hills could be assigned to H. hoolock. Our mitogenome analysis supported this conclusion. We estimate that gibbon divergence from a common ancestor occurred 8.38 mya and that the split between H. hoolock and H. leuconedys occurred 1.49 mya. These findings will facilitate exchange of individuals from different zoos for captive breeding programs and conservation and management of wild populations of these gibbons.
... Primarily on the basis of their karyotypes, gibbons are now divided into four major genera, with Nomascus, Symphalangus, Hylobates and Hoolock each possessing 52, 50, 44, and 38 diploid chromosomes, respectively. While many genetic studies have been performed, including a number based on karyotypes (GEISSMANN 2002;MÜLLER et al. 2003), mitochondrial DNA (HAYASHI et al. 1995;TAKACS et al. 2005;MONDA et al. 2007;WHITTAKER et al. 2007; VAN NGOC et al. 2010;MATSUDAIRA and ISHIDA 2010), Y chromosomes (CHAN et al. 2012), ALU repeats (GEISSMANN 2002;MEYER et al. 2012), and short stretches of autosomal sequence (FUENTES 2000;MOOTNICK 2006;KIM et al. 2011;WALL et al. 2013), the phylogenetic relationships among the four gibbon genera remain unresolved, with at least seven different topologies being supported by different data. ...
Gibbons are believed to have diverged from the larger great apes ~16.8 Mya and today reside in the rainforests of Southeast Asia. Based on their diploid chromosome number, the family Hylobatidae is divided into four genera, Nomascus , Symphalangus , Hoolock and Hylobates . Genetic studies attempting to elucidate the phylogenetic relationships among gibbons using karyotypes, mtDNA, the Y chromosome, and short autosomal sequences have been inconclusive. To examine the relationships among gibbon genera in more depth, we performed 2nd generation whole genome sequencing to a mean of ~15X coverage in two individuals from each genus. We developed a coalescent-based Approximate Bayesian Computation method incorporating a model of sequencing error generated by high coverage exome validation to infer the branching order, divergence times, and effective population sizes of gibbon taxa. Although Hoolock and Symphalangus are likely sister taxa, we could not confidently resolve a single bifurcating tree despite the large amount of data analyzed. Our combined results support the hypothesis that all four gibbon genera diverged at approximately the same time. Assuming an autosomal mutation rate of 1x10-9/site/year this speciation process occurred ~5 Mya during a period in the Early Pliocene characterized by climatic shifts and fragmentation of the Sunda shelf forests. Whole genome sequencing of additional individuals will be vital for inferring the extent of gene flow among species after the separation of the gibbon genera.
... The TPRT mechanism is considered unidirectional such that the absence of insertion is, by default, the ancestral state; conversely, shared insertions with matching TSDs are accepted as being inherited from a common ancestor. These unique attributes have made Alu elements well-established diagnostic molecular markers for the study of primate population genetic and phylogenetic relationships [16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31]. ...
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.
... A recent study conducted on populations of S. libidinosus, a species considered "Near Threatened" [12], emphasized that there is currently a lack of developed genetic systems available to study capuchin population and conservation genetics [13]. Primate specific Alu retrotransposons are well-established diagnostic genetic markers for the study of population genetic and phylogenetic relationships [15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31]. Nonautonomous Alu elements mobilize via a "copy and paste" mechanism through an RNA intermediate, utilizing the enzymatic machinery of autonomous LINE (L1) elements. ...
Capuchins are platyrrhines (monkeys found in the Americas) within the Cebidae family. For most of their taxonomic history, the two main morphological types of capuchins, gracile (untufted) and robust (tufted), were assigned to a single genus, Cebus. Further, all tufted capuchins were assigned to a single species, Cebus apella, despite broad geographic ranges spanning Central and northern South America. In 2012, tufted capuchins were assigned to their genus, Sapajus, with eight currently recognized species and five Cebus species, although these numbers are still under debate. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. However, Alu elements have rarely been used to study capuchins. Recent genome-level assemblies for capuchins (Cebus imitator; [Cebus_imitator_1.0] and Sapajus apella [GSC_monkey_1.0]) facilitated large scale ascertainment of young lineage-specific Alu insertions. There are 1607 capuchin specific and 678 Sapajus specific Alu insertions along with candidate oligonucleotides for locus-specific PCR assays for many elements. PCR analyses identified 104 genus level and 51 species level Alu insertion polymorphisms. The Alu datasets reported in this study provide a valuable resource that will assist in the classification of archival samples lacking phenotypic data and for the study of capuchin phylogenetic relationships.
... These four subgenera were subsequently raised to generic status Geissmann, 2002), and are now commonly recognised (e.g. Meyer et al., 2012;Takacs et al., 2005). Groves, therefore played a fundamental role in development of the currently understood systematics of the Hylobatidae at the generic level. ...
... The first two of these higher incidences might be explained by the longer lengths of the ancestral internodes leading to Catarrhini and hominoids, both leaving substantial times for the occurrence and fixation of gene conversion events. The increased gene conversion events in gibbons might be partially explained by the more highly active gibbon-specific AluY elements (AluYd3a1_gib [28]), which contain the same diagnostic deletion as the AluYc element. ...
The process of non-allelic gene conversion acts on homologous sequences during recombination, replacing parts of one with the other to make them uniform. Such concerted evolution is best described as paralogous ribosomal RNA gene unification that serves to preserve the essential house-keeping functions of the converted genes. Transposed elements (TE), especially Alu short interspersed elements (SINE) that have more than a million copies in primate genomes, are a significant source of homologous units and a verified target of gene conversion. The consequences of such a recombination-based process are diverse, including multiplications of functional TE internal binding domains and, for evolutionists, confusing divergent annotations of orthologous transposable elements in related species. We systematically extracted and compared 68,097 Alu insertions in various primates looking for potential events of TE gene conversion and discovered 98 clear cases of Alu–Alu gene conversion, including 64 cases for which the direction of conversion was identified (e.g., AluS conversion to AluY). Gene conversion also does not necessarily affect the entire homologous sequence, and we detected 69 cases of partial gene conversion that resulted in virtual hybrids of two elements. Phylogenetic screening of gene-converted Alus revealed three clear hotspots of the process in the ancestors of Catarrhini, Hominoidea, and gibbons. In general, our systematic screening of orthologous primate loci for gene-converted TEs provides a new strategy and view of a post-integrative process that changes the identities of such elements.
... Primate specific Alu retrotransposons are wellestablished genomic markers for the study of population genetic and phylogenetic relationships [27,[29][30][31][32][33][34][35][36][37][38][39][40]. Alu element insertions are considered unique events, have a known directionality where the ancestral state is known to be the absence of the element, and are relatively inexpensive to genotype [33,[41][42][43][44][45]. ...
Hylobatids (gibbons and siamangs) are the smallest of the apes distinguished by their coordinated duets, territorial songs, arm-swinging locomotion, and small family group sizes. Although they are the most speciose of the apes boasting twenty species living in eleven countries, ninety-five percent are critically endangered or endangered according to the IUCN's Red List of Threatened Species. Despite this, gibbons are often referred to as being 'forgotten' in the shadow of their great ape cousins because comparably they receive less research, funding and conservation attention. This is only the third book since the 1980s devoted to gibbons, and presents cutting-edge research covering a wide variety of topics including hylobatid ecology, conservation, phylogenetics and taxonomy. Written by gibbon researchers and practitioners from across the world, the book discusses conservation challenges in the Anthropocene and presents practice-based approaches and strategies to save these singing, swinging apes from extinction.
Transpositions of Alu sequences, representing the most abundant primate short interspersed elements (SINE), were evaluated as molecular cladistic markers to analyze the phylogenetic affiliations among the primate infraorders. Altogether 118 human loci, containing intronic Alu elements, were PCR analyzed for the presence of Alu sequences at orthologous sites in each of two strepsirhine, New World and Old World monkey species, Tarsius bancanus, and a nonprimate outgroup. Fourteen size-polymorphic amplification patterns exhibited longer fragments for the anthropoids (New World and Old World monkeys) and T. bancanus whereas shorter fragments were detected for the strepsirhines and the outgroup. From these, subsequent sequence analyses revealed three Alu transpositions, which can be regarded as shared derived molecular characters linking tarsiers and anthropoid primates. Concerning the other loci, scenarios are represented in which different SINE transpositions occurred independently in the same intron on the lineages leading both to the common ancestor of anthropoids and to T. bancanus, albeit at different nucleotide positions. Our results demonstrate the efficiency and possible pitfalls of SINE transpositions used as molecular cladistic markers in tracing back a divergence point in primate evolution over 40 million years old. The three Alu insertions characterized underpin the monophyly of haplorhine primates (Anthropoidea and Tarsioidea) from a novel perspective.
The human genome holds an extraordinary trove of information about human development, physiology, medicine and evolution.
Here we report the results of an international collaboration to produce and make freely available a draft sequence of the human
genome. We also present an initial analysis of the data, describing some of the insights that can be gleaned from the sequence.
Here we present a draft genome sequence of the common chimpanzee (
Pan troglodytes). Through comparison with the human genome, we have generated a largely complete catalogue of the genetic differences that have accumulated since the human and chimpanzee species diverged from our common ancestor, constituting approximately thirty-five million single-nucleotide changes, five million insertion/deletion events, and various chromosomal rearrangements. We use this catalogue to explore the magnitude and regional variation of mutational forces shaping these two genomes, and the strength of positive and negative selection acting on their genes. In particular, we find that the patterns of evolution in human and chimpanzee protein-coding genes are highly correlated and dominated by the fixation of neutral and slightly deleterious alleles. We also use the chimpanzee genome as an outgroup to investigate human population genetics and identify signatures of selective sweeps in recent human evolution. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
— We studied sequence variation in 16S rDNA in 204 individuals from 37 populations of the land snail Candidula unifasciata (Poiret 1801) across the core species range in France, Switzerland, and Germany. Phylogeographic, nested clade, and coalescence analyses were used to elucidate the species evolutionary history. The study revealed the presence of two major evolutionary lineages that evolved in separate refuges in southeast France as result of previous fragmentation during the Pleistocene. Applying a recent extension of the nested clade analysis (Templeton 2001), we inferred that range expansions along river valleys in independent corridors to the north led eventually to a secondary contact zone of the major clades around the Geneva Basin. There is evidence supporting the idea that the formation of the secondary contact zone and the colonization of Germany might be postglacial events. The phylogeographic history inferred for C. unifasciata differs from general biogeographic patterns of postglacial colonization previously identified for other taxa, and it might represent a common model for species with restricted dispersal.
Analyzing vertebrate genomes requires rapid mRNA/DNA and cross-species protein alignments. A new tool, BLAT, is more accurate and 500 times faster than popular existing tools for mRNA/DNA alignments and 50 times faster for protein alignments at sensitivity settings typically used when comparing vertebrate sequences. BLAT's speed stems from an index of all nonoverlapping K-mers in the genome. This index fits inside the RAM of inexpensive computers, and need only be computed once for each genome assembly. BLAT has several major stages. It uses the index to find regions in the genome likely to be homologous to the query sequence. It performs an alignment between homologous regions. It stitches together these aligned regions (often exons) into larger alignments (typically genes). Finally, BLAT revisits small internal exons possibly missed at the first stage and adjusts large gap boundaries that have canonical splice sites where feasible. This paper describes how BLAT was optimized. Effects on speed and sensitivity are explored for various K-mer sizes, mismatch schemes, and number of required index matches. BLAT is compared with other alignment programs on various test sets and then used in several genome-wide applications. http://genome.ucsc.edu hosts a web-basedBLAT server for the human genome.
Gibbons, Family Hylobatidae Gray, 1870, are small, arboreal apes of the tropical and semi-deciduous forests of southeast Asia and parts of south and east Asia. Four genera and about 14 species are currently recognized; a number of them threatened with extinction. Two of the reasons for breeding gibbons in captivity are to retain species and subspecies diversity and to create a viable gene pool, with the ultimate goal of releasing animals into protected native habitat. Accurate taxonomic identification may be complicated for some gibbon species due to (1) variation in coat color, (2) sexual dichromatism, and (3) the occurrence of coat color changes from infancy through sexual maturity, and for all species because of (4) the impacts of such as malnutrition and housing on coloration (for example, their maintenance indoors only or in full sunlight), (5) the ease with which the vocalizations of the different species can be confused, (6) the difficulties in distinguishing some gibbon subspecies from each other, and (7) errors in, or the lack of, information concerning the origin of confiscated gibbons. Given these problems, it is not surprising that rescue and breeding centers encounter difficulties in identifying the gibbons they receive. I review the characteristics and identifying features of the species and subspecies of gibbons, including information from museum specimens, live gibbons housed at the Gibbon Conservation Center, Santa Clarita, California, and a number of zoos worldwide.