RESUMEN
The Javan gibbon (Hylobatesmoloch) is endemic to the island of Java and its distribution is restricted from the western tip of Java to the Dieng Mountains in Central Java. Unlike the other known habitats that hold a large population of Javan gibbons, the Dieng Mountains have not been protected and experience various threats. This study, which was conducted in 2018 and 2021, aimed to provide an update of the current density and population size of Javan gibbons in Dieng after the most recent study in 2010 and to investigate their relationships with habitat characteristics (vegetation and elevation). The triangulation method and a new acoustic spatial capture-recapture method were used to estimate group density. A new approach for extrapolation, based on the habitat suitability model, was also developed to calculate population size. The results show that the Javan gibbon population in the Dieng Mountains has most likely increased. The mean group density in each habitat type was high: 2.15 groups/km2 in the low suitable habitat and 5.55 groups/km2 in the high suitable habitat. The mean group size (3.95 groups/km2, n = 20) was higher than those reported in previous studies. The overall population size was estimated to be 1092 gibbons. This population increase might indicate the success of conservation efforts during the last decade. However, more effort should be made to ensure the long-term future of this threatened species. Although the density significantly differed between habitat suitability types, it was not influenced by the vegetation structure or elevation. A combination of multiple variables will probably have a greater effect on density variation.
RESUMEN
In this study, we present the first genetic evidence of the phylogenetic position of Tarsius pumilus, the mountain tarsier of Sulawesi, Indonesia. This mysterious primate is the only Eastern tarsier species that occurs exclusively in cloud forests above 1800 m.a.s.l. It exhibits striking morphological peculiarities-most prominently its extremely reduced body size, which led to the common name of 'pygmy tarsier'. However, our results indicate that T. pumilus is not an aberrant form of a lowland tarsier, but in fact, the most basal of all Sulawesi tarsiers. Applying a Bayesian multi-locus coalescent approach, we dated the divergence between the T. pumilus lineage and the ancestor of all other extant Sulawesi tarsiers to 9.88 Mya. This is as deep as the split between the two other tarsier genera Carlito (Philippine tarsiers) and Cephalopachus (Western tarsiers), and predates further tarsier diversification on Sulawesi by around 7 Myr. The date coincides with the deepening of the marine environment between eastern and western Sulawesi, which likely led to allopatric speciation between T. pumilus or its predecessor in the west and the ancestor of all other Sulawesi tarsiers in the east. As the split preceded the emergence of permanent mountains in western Sulawesi, it is unlikely that the shift to montane habitat has driven the formation of the T. pumilus lineage.
Asunto(s)
Tarsiidae , Animales , Teorema de Bayes , Indonesia , Filogenia , Tarsiidae/genéticaRESUMEN
Conservation strategies are rarely systematically evaluated, which reduces transparency, hinders the cost-effective deployment of resources, and hides what works best in different contexts. Using data on the iconic and critically endangered orangutan (Pongo spp.), we developed a novel spatiotemporal framework for evaluating conservation investments. We show that around USD 1 billion was invested between 2000 and 2019 into orangutan conservation by governments, nongovernmental organizations, companies, and communities. Broken down by allocation to different conservation strategies, we find that habitat protection, patrolling, and public outreach had the greatest return on investment for maintaining orangutan populations. Given the variability in threats, land-use opportunity costs, and baseline remunerations in different regions, there were differential benefits per dollar invested across conservation activities and regions. We show that although challenging from a data and analysis perspective, it is possible to fully understand the relationships between conservation investments and outcomes and the external factors that influence these outcomes. Such analyses can provide improved guidance toward a more effective biodiversity conservation. Insights into the spatiotemporal interplays between the costs and benefits driving effectiveness can inform decisions about the most suitable orangutan conservation strategies for halting population declines. Although our study focuses on the three extant orangutan species of Sumatra and Borneo, our findings have broad application for evidence-based conservation science and practice worldwide.
Asunto(s)
Especies en Peligro de Extinción , Pongo , Animales , Conservación de los Recursos Naturales , Indonesia , Pongo pygmaeus , Dinámica PoblacionalRESUMEN
High social status is the primary determinant of reproductive success among group-living male mammals. Primates living in multimale-multifemale groups show the greatest variation in the strength of this link, with marked variation in reproductive skew by male dominance among species, dependent on the degree of female fertile phase synchrony, and the number of competing males. Here, we present data on two groups of wild crested macaques (Macaca nigra), living in the Tangkoko Reserve, Sulawesi, Indonesia. We investigated male monopolization of fertile females in 31 cycles of 19 females, and genetic paternity of 14 offspring conceived during the study period. We show that female fertile phase synchrony was low, that females had few mating partners in their fertile phase, and that dominant males monopolized a high proportion of consortships and matings, resulting in marked and steep mating and reproductive skew. We conclude that female cycle asynchrony provides the opportunity for strong direct male-male competition in crested macaques, resulting in monopolization of females by dominant males, consistent with their marked sexual dimorphism. Our study provides a test of the underlying factors that determine the relative occurrence and strength of different mechanisms of sexual selection, and the phenotypes that evolve as a result.
Asunto(s)
Fertilidad , Macaca/fisiología , Conducta Sexual Animal , Animales , Ciclo Estral , Femenino , Masculino , Reproducción , Predominio SocialRESUMEN
Habitat loss and hunting are major threats to the long-term survival of the viable orangutan population in Batang Toru. East Batang Toru Forest Block (EBTFB) is the most threatened area due to low forest cover and high encroachment. Based on a preliminary survey in 2008, Hopong forest which is located in EBTFB, had the highest orangutan density (0.7 ind/km2). However illegal logging and hunting of protected species were occuring in this unprotected forest. Since this location has been gazetted as unprotected forest from the first survey until this study was conducted, it is important to assess orangutans population trends. This study aims to provide an updated density of orangutan in Hopong forest. The study included the location of the original survey but covered a wider overall area. The line transect method was used to record orangutan nests, ficus and trees bearing fruits. A quadrat method was used to record vegetation. The encounter rate of orangutan declined from 0.7 ind/km2 to 0.4 ind/km2 between 2008 and 2015. Forest cover has also changed in the seven years between surveys and this has influenced orangutan and orangutan nest encounter rates in Hopong. Since unprotected forest is at more risk in comparison with protected forest, allocation status of the Hopong forest is critical to reduce the threats it faces.
RESUMEN
Six extant species of non-human great apes are currently recognized: Sumatran and Bornean orangutans, eastern and western gorillas, and chimpanzees and bonobos [1]. However, large gaps remain in our knowledge of fine-scale variation in hominoid morphology, behavior, and genetics, and aspects of great ape taxonomy remain in flux. This is particularly true for orangutans (genus: Pongo), the only Asian great apes and phylogenetically our most distant relatives among extant hominids [1]. Designation of Bornean and Sumatran orangutans, P. pygmaeus (Linnaeus 1760) and P. abelii (Lesson 1827), as distinct species occurred in 2001 [1, 2]. Here, we show that an isolated population from Batang Toru, at the southernmost range limit of extant Sumatran orangutans south of Lake Toba, is distinct from other northern Sumatran and Bornean populations. By comparing cranio-mandibular and dental characters of an orangutan killed in a human-animal conflict to those of 33 adult male orangutans of a similar developmental stage, we found consistent differences between the Batang Toru individual and other extant Ponginae. Our analyses of 37 orangutan genomes provided a second line of evidence. Model-based approaches revealed that the deepest split in the evolutionary history of extant orangutans occurred â¼3.38 mya between the Batang Toru population and those to the north of Lake Toba, whereas both currently recognized species separated much later, about 674 kya. Our combined analyses support a new classification of orangutans into three extant species. The new species, Pongo tapanuliensis, encompasses the Batang Toru population, of which fewer than 800 individuals survive. VIDEO ABSTRACT.
Asunto(s)
Especiación Genética , Pongo/genética , Animales , Conducta Animal/fisiología , Evolución Biológica , Especies en Peligro de Extinción , Flujo Génico/genética , Variación Genética , Genoma , Genómica , Hominidae/genética , Metagenómica/métodos , Filogenia , Pongo/clasificación , Pongo/fisiología , Pongo abelii/genética , Pongo pygmaeus/genéticaRESUMEN
Genetic analyses based on noninvasively collected samples have become an important tool for evolutionary biology and conservation. Crested macaques (Macaca nigra), endemic to Sulawesi, Indonesia, are important for our understanding of primate evolution as Sulawesi macaques represent an exceptional example of primate adaptive radiation. Crested macaques are also Critically Endangered. However, to date we know very little about their genetics. The aim of our study was to find and validate microsatellite markers useful for evolutionary, conservation, and other genetic studies on wild crested macaques. Using fecal samples of 176 wild macaques living in the Tangkoko Reserve, Sulawesi, we identified 12 polymorphic microsatellite loci through cross-species polymerase chain reaction amplification with later modification of some of these primers. We tested their suitability by investigating and exploring patterns of paternity, observed heterozygosity, and evidence for inbreeding. We assigned paternity to 63 of 65 infants with high confidence. Among cases with solved paternity, we found no evidence of extragroup paternity and natal breeding. We found a relatively steep male reproductive skew B index of 0.330 ± 0.267; mean ± SD) and mean alpha paternity of 65% per year with large variation across groups and years (29-100%). Finally, we detected an excess in observed heterozygosity and no evidence of inbreeding across our three study groups, with an observed heterozygosity of 0.766 ± 0.059 and expected heterozygosity of 0.708 ± 0.059, and an inbreeding coefficient of -0.082 ± 0.035. Our results indicate that the selected markers are useful for genetic studies on wild crested macaques, and possibly also on other Sulawesi and closely related macaques. They further suggest that the Tangkoko population of crested macaques is still genetically variable despite its small size, isolation, and the species' reproductive patterns. This gives us hope that other endangered primate species living in small, isolated populations may also retain a healthy gene pool, at least in the short term.
RESUMEN
PRDM9 is currently the sole speciation gene found in vertebrates causing hybrid sterility probably due to incompatible alleles. Its role in defining the double strand break loci during the meiotic prophase I is crucial for proper chromosome segregation. Therefore, the rapid turnover of the loci determining zinc finger array seems to be causative for incompatibilities. We here investigated the zinc finger domain-containing exon of PRDM9 in 23 tarsiers. Tarsiers, the most basal extant haplorhine primates, exhibit two frameshifting indels at the 5'-end of the array. The first mutation event interrupts the reading frame and function while the second compensates both. The fixation of this allele variant in tarsiers led to hypothesize that de- and reactivation of the zinc finger domain drove the speciation in early haplorhine or tarsiiform primates. Moreover, the high allelic diversity within Tarsius points to multiple effects of genetic drift reflecting their phylogeographic history since the Miocene.
Asunto(s)
Evolución Molecular , N-Metiltransferasa de Histona-Lisina/genética , Mutación INDEL , Tarsiidae/genética , Animales , Dominios Proteicos , Dedos de ZincRESUMEN
ABSTRACT: In promiscuous primates, interactions between adult males and infants have rarely been investigated. However, recent evidence suggests that male affiliation towards infants has an influence on several aspects of the infants' life. Furthermore, affiliations may be associated with male reproductive strategy. In this study, we examined which social factors influenced male-infant affiliation initiated by either male or infant, in wild crested macaques (Macaca nigra). We combined behavioral data and genetic paternity analysis from 30 infants living in three wild groups in Tangkoko Reserve, Indonesia. Our results indicate that adult males and infants do not interact at random, but rather form preferential associations. The social factors with the highest influence on infant-initiated interactions were male rank and male association with the infant's mother. While infants initiated affiliations with males more often in the absence of their mothers, adult males initiated more affiliations with infants when their mothers were present. Furthermore, males initiated affiliations more often when they were in the same group at the time the infant was conceived, when they held a high dominance rank, or when they had a close relationship with the mother. Interestingly, paternity did not affect male-infant affiliation despite being highly skewed in this species. Overall, our results suggest that adult males potentially associate with an infant to secure future mating with the mother. Infants are more likely to associate with a male to receive better support, suggesting a strategy to increase the chance of infant survival in a primate society with high infant mortality. SIGNIFICANCE STATEMENT: We explore social relationships between males and infants in a promiscuous primate, the wild crested macaque. Our novel approach addresses the nature of affiliations both from males' and infants' perspectives. The results show that males and infants form preferential associations. Male-female affiliation, but not paternity, was a significant predictor of interactions initiated both by males and infants. Males initiated more interactions towards infants when the mother was in proximity, while infants initiated more interactions in her absence. Finally, high-ranking males were more likely to initiate interactions towards infants. We demonstrated that paternity is not a good predictor of male-infant affiliations, even in a species with a high reproductive skew and a relatively high confidence of paternity. Our paper is one of the first to show that infants are active agents in establishing and maintaining preferential relationships with males.
RESUMEN
The Indonesian island of Sulawesi harbors a highly endemic and diverse fauna sparking fascination since long before Wallace's contemplation of biogeographical patterns in the region. Allopatric diversification driven by geological or climatic processes has been identified as the main mechanism shaping present faunal distribution on the island. There is both consensus and conflict among range patterns of terrestrial species pointing to the different effects of vicariant events on once co-distributed taxa. Tarsiers, small nocturnal primates with possible evidence of an Eocene fossil record on the Asian mainland, are at present exclusively found in insular Southeast Asia. Sulawesi is hotspot of tarsier diversity, whereby island colonization and subsequent radiation of this old endemic primate lineage remained largely enigmatic. To resolve the phylogeographic history of Sulawesi tarsiers we analyzed an island-wide sample for a set of five approved autosomal phylogenetic markers (ABCA1, ADORA3, AXIN1, RAG1, and TTR) and the paternally inherited SRY gene. We constructed ML and Bayesian phylogenetic trees and estimated divergence times between tarsier populations. We found that their arrival at the Proto-Sulawesi archipelago coincided with initial Miocene tectonic uplift and hypothesize that tarsiers dispersed over the region in distinct waves. Intra-island diversification was spurred by land emergence and a rapid succession of glacial cycles during the Plio-Pleistocene. Some tarsier range boundaries concur with spatial limits in other taxa backing the notion of centers of faunal endemism on Sulawesi. This congruence, however, has partially been superimposed by taxon-specific dispersal patterns.
Asunto(s)
Biodiversidad , Oceanografía , Tarsiidae/clasificación , Animales , Indonesia , Datos de Secuencia Molecular , Tarsiidae/genéticaRESUMEN
Premature loss of offspring decreases direct fitness of parents. In gregarious mammals, both ecological and social variables impact offspring survival and may interact with each other in this regard. Although a number of studies have investigated factors influencing offspring loss in mammals, we still know very little on how different factors interact with one another. We therefore investigated fetal and infant mortality in 3 large groups of wild crested macaques (Macaca nigra) over a period of up to 5 years by including potential social causes such as maternal dominance rank, male immigration, between group encounters, and ecological conditions such as rainfall in a multivariate survival analysis using Cox proportional hazards model. Infant but not fetal survival was most impaired after a recent takeover of the alpha-male position by an immigrant male. Furthermore, infant survival probability increased when there was an increase in number of group adult females and rainfall. Fetal survival probability also increased with an increase of these 2 factors, but more in high-ranking than low-ranking females. Fetal survival, unlike that of infants, was also improved by an increase of intergroup encounter rates. Our study thus stresses the importance of survival analyses using a multivariate approach and encompassing more than a single offspring stage to investigate the determinants of female direct fitness. We further provide evidence for fitness costs and benefits of group living, possibly deriving from high pressures of both within- and between-group competition, in a wild primate population.
RESUMEN
Patterns and processes of molecular evolution critically influence inferences in phylogeny and phylogeography. Within primates, a shift in evolutionary rates has been identified as the rationale for contrasting findings from mitochondrial and nuclear DNA studies as to the position of Tarsius. While the latter now seems settled, we sequenced complete mitochondrial genomes of three Sulawesi tarsiers (Tarsius dentatus, T. lariang, and T. wallacei) and analyzed substitution rates among tarsiers and other primates to infer driving processes of molecular evolution. We found substantial length polymorphism of the D-loop within tarsier individuals, but little variation of predominant lengths among them, regardless of species. Length variation was due to repetitive elements in the CSB domain-minisatellite motifs of 35 bp length and microsatellite motifs of 6 bp length. Amino acid evolutionary rates were second highest among major primate taxa relative to nucleotide substitution rates. We observed many radical possibly function-altering amino acid changes that were rarely driven by positive selection and thus potentially slightly deleterious or neutral. We hypothesize that the observed pattern of an increased amino acid evolutionary rate in tarsier mitochondrial genomes may be caused by hitchhiking of slightly deleterious mutations with favored D-loop length variants selected for maximizing replication success within the cell or the mitochondrion.
Asunto(s)
Evolución Molecular , Genoma Mitocondrial , Tarsiidae/genética , Animales , ADN Mitocondrial/genética , Repeticiones de Microsatélite , Repeticiones de Minisatélite , Filogenia , Selección Genética , Análisis de Secuencia de ADNRESUMEN
A multitude of factors influence how natural populations are genetically structured, including dispersal barriers, inhomogeneous habitats, and social organization. Such population subdivision is of special concern in endangered species, as it may lead to reduced adaptive potential and inbreeding in local subpopulations, thus increasing the risk of future extinctions. With only 6600 animals left in the wild, Sumatran orangutans (Pongo abelii) are among the most endangered, but also most enigmatic, great ape species. In order to infer the fine-scale population structure and connectivity of Sumatran orangutans, we analyzed the most comprehensive set of samples to date, including mitochondrial hyper-variable region I haplotypes for 123 individuals and genotypes of 27 autosomal microsatellite markers for 109 individuals. For both mitochondrial and autosomal markers, we found a pronounced population structure, caused by major rivers, mountain ridges, and the Toba caldera. We found that genetic diversity and corresponding long-term effective population size estimates vary strongly among sampling regions for mitochondrial DNA, but show remarkable similarity for autosomal markers, hinting at male-driven long-distance gene flow. In support of this, we identified several individuals that were most likely sired by males originating from other genetic clusters. Our results highlight the effect of natural barriers in shaping the genetic structure of great ape populations, but also point toward important dispersal corridors on northern Sumatra that allow for genetic exchange.
Asunto(s)
Migración Animal , Especies en Peligro de Extinción , Flujo Génico/genética , Variación Genética , Genética de Población , Pongo abelii/fisiología , Animales , Secuencia de Bases , ADN Mitocondrial/genética , Heces/química , Geografía , Cabello/química , Haplotipos/genética , Indonesia , Repeticiones de Microsatélite/genética , Datos de Secuencia Molecular , Polimorfismo de Longitud del Fragmento de Restricción , Pongo abelii/genética , Densidad de Población , Dinámica Poblacional , Reacción en Cadena en Tiempo Real de la Polimerasa , Análisis de Secuencia de ADNRESUMEN
BACKGROUND: Female signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females' interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour. RESULTS: We show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this. CONCLUSION: Though probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may in part be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.
Asunto(s)
Evolución Biológica , Fertilidad , Macaca/fisiología , Conducta Sexual Animal , Animales , Femenino , Genitales Femeninos , Masculino , Ovulación , Predominio SocialRESUMEN
Philopatry and sex-biased dispersal have a strong influence on population genetic structure, so the study of species dispersal patterns and evolutionary mechanisms shaping them are of great interest. Particularly nongregarious mammalian species present an underexplored field of study: despite their lower levels of sociality compared to group-living species, interactions among individuals do occur, providing opportunities for cryptic kin selection. Among the least gregarious primates are orang-utans (genus: Pongo), in which preferential associations among females have nevertheless been observed, but for which the presence of kin structures was so far unresolved because of the equivocal results of previous genetic studies. To clarify relatedness and dispersal patterns in orang-utans, we examined the largest longitudinal set of individuals with combined genetic, spatial and behavioural data. We found that males had significantly higher mitochondrial DNA (mtDNA) variation and more unique haplotypes, thus underscoring their different maternal ancestries compared to females. Moreover, pedigree reconstruction based on 24 highly polymorphic microsatellite markers and mtDNA haplotypes demonstrated the presence of three matrilineal clusters of generally highly related females with substantially overlapping ranges. In orang-utans and possibly other nongregarious species, comparing average biparental relatedness (r) of males and females to infer sex-biased dispersal is extremely problematic. This is because the opportunistic sampling regime frequently employed in nongregarious species, combined with overlapping space use of distinct matrilineal clusters, leads to a strong downward bias when mtDNA lineage membership is ignored. Thus, in nongregarious species, correct inferences of dispersal can only be achieved by combining several genetic approaches with detailed spatial information.
Asunto(s)
Variación Genética , Genética de Población , Pongo pygmaeus/genética , Animales , ADN Mitocondrial/genética , Femenino , Haplotipos , Masculino , Datos de Secuencia Molecular , Linaje , Análisis de Secuencia de ADNRESUMEN
BACKGROUND: Several studies suggested great ape cultures, arguing that human cumulative culture presumably evolved from such a foundation. These focused on conspicuous behaviours, and showed rich geographic variation, which could not be attributed to known ecological or genetic differences. Although geographic variation within call types (accents) has previously been reported for orang-utans and other primate species, we examine geographic variation in the presence/absence of discrete call types (dialects). Because orang-utans have been shown to have geographic variation that is not completely explicable by genetic or ecological factors we hypothesized that this will be similar in the call domain and predict that discrete call type variation between populations will be found. METHODOLOGY/PRINCIPAL FINDINGS: We examined long-term behavioural data from five orang-utan populations and collected fecal samples for genetic analyses. We show that there is geographic variation in the presence of discrete types of calls. In exactly the same behavioural context (nest building and infant retrieval), individuals in different wild populations customarily emit either qualitatively different calls or calls in some but not in others. By comparing patterns in call-type and genetic similarity, we suggest that the observed variation is not likely to be explained by genetic or ecological differences. CONCLUSION/SIGNIFICANCE: These results are consistent with the potential presence of 'call cultures' and suggest that wild orang-utans possess the ability to invent arbitrary calls, which spread through social learning. These findings differ substantially from those that have been reported for primates before. First, the results reported here are on dialect and not on accent. Second, this study presents cases of production learning whereas most primate studies on vocal learning were cases of contextual learning. We conclude with speculating on how these findings might assist in bridging the gap between vocal communication in non-human primates and human speech.
Asunto(s)
Evolución Biológica , ADN Mitocondrial/genética , Aprendizaje , Pongo , Vocalización Animal , Animales , Genética de Población/métodos , Genotipo , Haplotipos , Humanos , Pongo/genética , Pongo/fisiología , Habla/fisiología , Vocalización Animal/fisiologíaRESUMEN
BACKGROUND: Routine trichromatic color vision is a characteristic feature of catarrhines (humans, apes and Old World monkeys). This is enabled by L and M opsin genes arrayed on the X chromosome and an autosomal S opsin gene. In non-human catarrhines, genetic variation affecting the color vision phenotype is reported to be absent or rare in both L and M opsin genes, despite the suggestion that gene conversion has homogenized the two genes. However, nucleotide variation of both introns and exons among catarrhines has only been examined in detail for the L opsin gene of humans and chimpanzees. In the present study, we examined the nucleotide variation of gibbon (Catarrhini, Hylobatidae) L and M opsin genes. Specifically, we focused on the 3.6~3.9-kb region that encompasses the centrally located exon 3 through exon 5, which encode the amino acid sites functional for the spectral tuning of the genes. RESULTS: Among 152 individuals representing three genera (Hylobates, Nomascus and Symphalangus), all had both L and M opsin genes and no L/M hybrid genes. Among 94 individuals subjected to the detailed DNA sequencing, the nucleotide divergence between L and M opsin genes in the exons was significantly higher than the divergence in introns in each species. The ratio of the inter-LM divergence to the intra-L/M polymorphism was significantly lower in the introns than that in synonymous sites. When we reconstructed the phylogenetic tree using the exon sequences, the L/M gene duplication was placed in the common ancestor of catarrhines, whereas when intron sequences were used, the gene duplications appeared multiple times in different species. Using the GENECONV program, we also detected that tracts of gene conversions between L and M opsin genes occurred mostly within the intron regions. CONCLUSIONS: These results indicate the historical accumulation of gene conversions between L and M opsin genes in the introns in gibbons. Our study provides further support for the homogenizing role of gene conversion between the L and M opsin genes and for the purifying selection against such homogenization in the central exons to maintain the spectral difference between L and M opsins in non-human catarrhines.
Asunto(s)
Conversión Génica , Hylobates/genética , Nucleótidos/genética , Opsinas/genética , Animales , Genotipo , Intrones , Filogenia , Polimorfismo GenéticoRESUMEN
BACKGROUND: Colobine monkeys constitute a diverse group of primates with major radiations in Africa and Asia. However, phylogenetic relationships among genera are under debate, and recent molecular studies with incomplete taxon-sampling revealed discordant gene trees. To solve the evolutionary history of colobine genera and to determine causes for possible gene tree incongruences, we combined presence/absence analysis of mobile elements with autosomal, X chromosomal, Y chromosomal and mitochondrial sequence data from all recognized colobine genera. RESULTS: Gene tree topologies and divergence age estimates derived from different markers were similar, but differed in placing Piliocolobus/Procolobus and langur genera among colobines. Although insufficient data, homoplasy and incomplete lineage sorting might all have contributed to the discordance among gene trees, hybridization is favored as the main cause of the observed discordance. We propose that African colobines are paraphyletic, but might later have experienced female introgression from Piliocolobus/Procolobus into Colobus. In the late Miocene, colobines invaded Eurasia and diversified into several lineages. Among Asian colobines, Semnopithecus diverged first, indicating langur paraphyly. However, unidirectional gene flow from Semnopithecus into Trachypithecus via male introgression followed by nuclear swamping might have occurred until the earliest Pleistocene. CONCLUSIONS: Overall, our study provides the most comprehensive view on colobine evolution to date and emphasizes that analyses of various molecular markers, such as mobile elements and sequence data from multiple loci, are crucial to better understand evolutionary relationships and to trace hybridization events. Our results also suggest that sex-specific dispersal patterns, promoted by a respective social organization of the species involved, can result in different hybridization scenarios.
Asunto(s)
Evolución Biológica , Núcleo Celular/genética , Colobinae/genética , ADN Mitocondrial/genética , Hibridación Genética , Filogenia , Elementos Alu , Animales , Mapeo Cromosómico , Colobinae/clasificación , Femenino , Masculino , Análisis de Secuencia de ADN , Cromosoma X/genética , Cromosoma Y/genéticaRESUMEN
The Southeast Asian Sunda archipelago harbors a rich biodiversity with a substantial proportion of endemic species. The evolutionary history of these species has been drastically influenced by environmental forces, such as fluctuating sea levels, climatic changes, and severe volcanic activities. Orangutans (genus: Pongo), the only Asian great apes, are well suited to study the relative impact of these forces due to their well-documented behavioral ecology, strict habitat requirements, and exceptionally slow life history. We investigated the phylogeographic patterns and evolutionary history of orangutans in the light of the complex geological and climatic history of the Sunda archipelago. Our study is based on the most extensive genetic sampling to date, covering the entire range of extant orangutan populations. Using data from three mitochondrial DNA (mtDNA) genes from 112 wild orangutans, we show that Sumatran orangutans, Pongo abelii, are paraphyletic with respect to Bornean orangutans (P. pygmaeus), the only other currently recognized species within this genus. The deepest split in the mtDNA phylogeny of orangutans occurs across the Toba caldera in northern Sumatra and, not as expected, between both islands. Until the recent past, the Toba region has experienced extensive volcanic activity, which has shaped the current phylogeographic patterns. Like their Bornean counterparts, Sumatran orangutans exhibit a strong, yet previously undocumented structuring into four geographical clusters. However, with 3.50 Ma, the Sumatran haplotypes have a much older coalescence than their Bornean counterparts (178 kya). In sharp contrast to the mtDNA data, 18 Y-chromosomal polymorphisms show a much more recent coalescence within Sumatra compared with Borneo. Moreover, the deep geographic structure evident in mtDNA is not reflected in the male population history, strongly suggesting male-biased dispersal. We conclude that volcanic activities have played an important role in the evolutionary history of orangutans and potentially of many other forest-dwelling Sundaland species. Furthermore, we demonstrate that a strong sex bias in dispersal can lead to conflicting patterns in uniparentally inherited markers even at a genus-wide scale, highlighting the need for a combined usage of maternally and paternally inherited marker systems in phylogenetic studies.