ABSTRACT
Sex-biased dispersal (SBD) is common in many vertebrates, including primates. However, dispersal patterns in New World primates may vary among closely related taxa or populations in different local environments. Here, we test for SBD in an endangered New World primate, the Central American Squirrel Monkey (Saimiri oerstedii citrinellus). Previous studies of behavioral ecology suggest predominantly female dispersal in S.o. oerstedii in the Southern Pacific region of Costa Rica. However, our genetic data do not support strongly female-biased dispersal in S.o. citrinellus in the Central Pacific region. Our tests for SBD using microsatellite data including comparisons of isolation-by-distance, AI(c) , and F(ST) values between males and females were not significant. Also, we found greater population genetic structure in mitochondrial markers than in microsatellite markers, indicative of predominantly male dispersal. We conclude that both sexes disperse in S.o. citrinellus, and that males probably disperse over longer distances. We discuss how spatial and temporal variation among local populations should be taken into account when studying dispersal patterns and especially sex bias.
Subject(s)
Behavior, Animal , DNA, Mitochondrial , Saimiri/genetics , Animals , Costa Rica , Female , Male , Microsatellite Repeats , Panama , Population Dynamics , Saimiri/physiology , Sequence Analysis, DNA , Sex FactorsABSTRACT
Southern India, one of the last strongholds of the endangered Asian elephant (Elephas maximus), harbours about one-fifth of the global population. We present here the first population genetic study of free-ranging Asian elephants, examining within- and among-population differentiation by analysing mitochondrial DNA (mtDNA) and nuclear microsatellite DNA differentiation across the Nilgiris-Eastern Ghats, Anamalai, and Periyar elephant reserves of southern India. Low mtDNA diversity and 'normal' microsatellite diversity were observed. Surprisingly, the Nilgiri population, which is the world's single largest Asian elephant population, had only one mtDNA haplotype and lower microsatellite diversity than the two other smaller populations examined. There was almost no mtDNA or microsatellite differentiation among localities within the Nilgiris, an area of about 15,000 km2. This suggests extensive gene flow in the past, which is compatible with the home ranges of several hundred square kilometres of elephants in southern India. Conversely, the Nilgiri population is genetically distinct at both mitochondrial and microsatellite markers from the two more southerly populations, Anamalai and Periyar, which in turn are not genetically differentiated from each other. The more southerly populations are separated from the Nilgiris by only a 40-km-wide stretch across a gap in the Western Ghats mountain range. These results variably indicate the importance of population bottlenecks, social organization, and biogeographic barriers in shaping the distribution of genetic variation among Asian elephant populations in southern India.
Subject(s)
DNA, Mitochondrial/genetics , Elephants/genetics , Genetic Variation , Genetics, Population , Microsatellite Repeats , Animals , Cell Nucleus/genetics , Elephants/classification , Evolution, Molecular , Geography , Haplotypes , India , Phylogeny , Polymorphism, GeneticABSTRACT
Noninvasive genotyping has not gained wide application, due to the notion that it is unreliable, and also because remedial measures are time consuming and expensive. Of the wide variety of noninvasive DNA sources, dung is the most universal and most widely used in studies. We have developed collection, extraction, and amplification protocols that are inexpensive and provide a high level of success in amplifying both mitochondrial and nuclear DNA from dung. Here we demonstrate the reliability of genotyping from elephant dung using these protocols by comparing results from dung-extracted DNA to results from blood-extracted DNA. The level of error from dung extractions was only slightly higher than from blood extractions, and conducting two extractions from each sample and a single amplification from each extraction was sufficient to eliminate error. Di-, tri-, and tetranucleotide loci were equally reliable, and low DNA quantity and quality and PCR inhibitors were not a major problem in genotyping from dung. We discuss the possible causes of error in genotyping with particular reference to noninvasive samples and suggest methods of reducing such error.
Subject(s)
Blood/metabolism , DNA/metabolism , Feces/chemistry , Sequence Analysis, DNA/methods , Animals , Elephants/genetics , Genotype , Microsatellite Repeats , Polymerase Chain ReactionABSTRACT
This study investigates hybridization and population genetics of two species of macaque monkey in Sulawesi, Indonesia, using molecular markers from mitochondrial, autosomal, and Y-chromosome DNA. Hybridization is the interbreeding of individuals from different parental taxa that are distinguishable by one or more heritable characteristics. Because hybridization can affect population structure of the parental taxa, it is an important consideration for conservation management. On the Indonesian island of Sulawesi an explosive diversification of macaques has occurred; seven of 19 species in the genus Macaca live on this island. The contact zone of the subjects of this study, M. maura and M. tonkeana, is located at the base of the southwestern peninsula of Sulawesi. Land conversion in Sulawesi is occurring at an alarming pace; currently two species of Sulawesi macaque, one of which is M. maura, are classified as endangered species. Results of this study indicate that hybridization among M. maura and M. tonkeana has led to different distributions of molecular variation in mitochondrial DNA and nuclear DNA in the contact zone; mitochondrial DNA shows a sharp transition from M. maura to M. tonkeana haplotypes, but nuclear DNA from the parental taxa is homogenized in a narrow hybrid zone. Similarly, within M. maura divergent mitochondrial DNA haplotypes are geographically structured but population subdivision in the nuclear genome is low or absent. In M. tonkeana, mitochondrial DNA haplotypes are geographically structured and a high level of nuclear DNA population subdivision is present in this species. These results are largely consistent with a macaque behavioral paradigm of female philopatry and obligate male dispersal, suggest that introgression between M. maura and M. tonkeana is restricted to the hybrid zone, and delineate one conservation management unit in M. maura and at least two in M. tonkeana.
Subject(s)
Genetics, Population , Macaca/genetics , Animals , Base Sequence , Behavior, Animal , DNA/analysis , DNA/genetics , DNA, Mitochondrial/analysis , DNA, Mitochondrial/genetics , Female , Genotype , Humans , Indonesia , Linkage Disequilibrium , Macaca/classification , Male , Microsatellite Repeats , Molecular Sequence Data , Phylogeny , Sequence Alignment , Y ChromosomeABSTRACT
We report here the results of one of the first analyses to use male-specific nuclear markers in elucidating primate phylogenetic relationships at the intrageneric level. Two closely linked Y chromosome markers, TSPY and SRY, were sequenced for a total of 3100 bases. Forty-four macaques, representing 18 of the 19 recognized species, were sequenced for the full 3.1 kb, as was 1 individual from each of the following outgroup genera: Papio, Theropithecus, Mandrillus, Allenopithecus,Cercopithecus, Trachypithecus, Presbytis, and Homo. In contrast to recent mtDNA phylogenies, Y chromosome loci support four monophyletic species groups, including a sinica group containing M. arctoides-a classification largely congruent with those of Fooden and Delson. Comparison of mtDNA and Y chromosome phylogenies highlight (1) a potential hybrid origin of Macaca arctoides from M. fascicularis and proto-M. assamensis/thibetana and (2) cases of mitochondrial paraphyly in macaque species whose Y chromosome lineages are monophyletic-a probable evolutionary consequence of philopatric females vs dispersing males. These results raise the question of whether a phylogenetic tree should be a topology of species origins or a depiction of more current species relationships, including subsequent episodes of introgression.
Subject(s)
DNA, Mitochondrial/genetics , Macaca/genetics , Nuclear Proteins , Transcription Factors , Y Chromosome/genetics , Animals , Cercopithecinae/classification , Cercopithecinae/genetics , DNA/chemistry , DNA/genetics , DNA-Binding Proteins/genetics , Evolution, Molecular , Female , Macaca/classification , Male , Molecular Sequence Data , Phylogeny , Sequence Analysis, DNA , Sex-Determining Region Y ProteinABSTRACT
Evolutionary geneticists have increasingly used sequence variation in mitochondrial DNA (mtDNA) as a source of historical information. However, conclusions based on these data remain tentative because a sufficiently clear understanding of the evolutionary dynamics of mtDNA has yet to be developed. In this paper we present the results of computer simulations designed to illustrate the effects of social structure, geographical structure, and population size on the rate of nucleotide substitution and lineage sorting of mtDNA. The model is based in part on the social structure of macaque monkeys. Simulated populations of females were divided into 25 social groups; the animals in each were distributed in a hierarchy of four dominance rank categories. The probabilities for offspring survivorship were varied among dominance ranks to reflect the fitness consequences of social structure. Population size was varied across runs from 100 to 300 females. The pattern of female migration was also varied to mimic either the island model or the stepping-stone model. All these variables are shown to affect the lineage sorting period (LSP), and certain combinations of parameter values can cause the retention of mtDNA polymorphisms for a very long time. In addition, the simulations exhibited a negative relationship between the LSP and substitution rate over a modest and realistic range of LSP values. An important implication of these results is that estimates of time since isolation based on the assumption of a constant molecular clock may be biased and unreliable.
Subject(s)
DNA, Mitochondrial/genetics , Evolution, Molecular , Genetics, Population , Macaca/genetics , Social Dominance , Animals , Cell Lineage , Computer Simulation , Emigration and Immigration , Female , Geography , Models, Genetic , Mutagenesis , Population Density , Time FactorsABSTRACT
The New World monkeys are divided into two main groups, Callitrichidae and Cebidae. Callimico goeldii shares traits with both the Cebidae and the Callitrichidae. Recent morphological phyletic studies generally place Callimico as the most basal member of the Callitrichidae. In contrast, genetic studies (immunological, restriction fragment, and sequence data) have consistently placed Callimico somewhere within the Callitrichidae, not basal to this clade. A DNA sequence data set from the terminal 236 codons of the mitochondrial ND4 gene and the tRNA(His), tRNA(Ser), and tRNA(Leu) genes was generated to clarify the position of Callimico. The sequences of 887 base pairs were analyzed by maximum-parsimony, neighbor-joining, and maximum-likelihood methods. The results of these various methods are generally congruent and place Callimico within the Callitrichidae between the marmosets (Callithrix and Cebuella) and the tamarins (Saguinus and Leontopithecus). Combined analyses of all suitable nuclear and mitochondrial gene sequences confirm the position of Callimico between the marmosets and the tamarins. As available molecular evidence indicates that Callimico is more closely related to the marmosets than to the tamarins, a reconsideration of the morphological evidence in light of the consensus tree from DNA sequence analyses is warranted. The marmosets and tamarins share four morphological characters (loss of the third molar, loss of the hypocone, reduced body size, reproductive twinning). Dwarfism may have evolved repeatedly among the Callitrichidae. It is well-known that the loss of a character can occur many times independently. The reproduction of marmosets and tamarins is extremely specialized and it is difficult to imagine that this complex and unique twinning system evolved separately in marmosets and tamarins. However, it is possible that a secondary reversal to single offspring took place in Callimico.
Subject(s)
Callimico/classification , Callimico/genetics , DNA, Mitochondrial/genetics , Evolution, Molecular , Animals , Callimico/anatomy & histology , Cebidae/anatomy & histology , Cebidae/genetics , Genetic Variation , Models, Genetic , Molecular Sequence Data , NADH Dehydrogenase/genetics , Phylogeny , Polymerase Chain Reaction , RNA/genetics , RNA, Mitochondrial , RNA, Ribosomal, 16S/genetics , RNA, Transfer, His/genetics , RNA, Transfer, Leu/genetics , RNA, Transfer, Ser/genetics , Saguinus/anatomy & histology , Saguinus/genetics , Sequence Analysis, DNAABSTRACT
Molecular phylogenetic relationships among all recognized species within the genus Macaca, were assessed using high-resolution restriction site mapping of the mitochondrial ribosomal genes. By outgroup comparisons to other members of the cercopithecine subfamily, the macaques appear to be a monophyletic assemblage. Within the genus, the relationships are in general consistent with previous genetic studies, though they are less concordant with the separation of the species into four distinct species groups based on modification of the genitalia. Our data support: (1) Macaca sylvanus as sister clade to all Asian macaques; (2) the silenus group as a monophyletic assemblage, with the Sulawesi macaques diverging and colonizing Sulawesi much earlier than previously thought; (3) the fascicularis group as a paraphyletic assemblage, including all non-silenus group Asian macaques; (4) the sinica group as a monophyletic assemblage, possibly derived from a fascicularis-like ancestor; and (5) Macaca arctoides as a separate lineage from the sinica group, also originating from a fascicularis-like ancestor. This study supports the notion that species with more specialized genitalia evolved from less derived taxa, and in general are in agreement with the dispersal scenarios proposed by Fooden (1980) and Delson (1980) for the macaques.
Subject(s)
DNA, Mitochondrial , Macaca/classification , Phylogeny , Animals , Animals, Wild , Animals, Zoo , Binding Sites , DNA, Ribosomal , Humans , Macaca/genetics , Restriction Mapping/methodsABSTRACT
Mitochondrial DNA variation was surveyed in nine populations of the pigtail macaque (Macaca nemestrina), covering all three recognized subspecies in Southeast Asia. To do this, a 2,300 base pair fragment spanning the mitochondrial NAD 3 and NAD 4 genes and flanking tRNA subunits leucine and glycine was targeted for amplification and digested with a battery of 16 restriction endonucleases. Out of a total of 107 individuals, 32 unique haplotypes could be distinguished. Parsimony and neighbor-joining analyses grouped the haplotypes into five strongly supported assemblages representing China/Thailand, Malaysia, Sumatra, Borneo, and Siberut. These results indicate that the mainland and island mtDNA haplotypes are strictly and uniquely limited to the geographic ranges of the recognized morphological subspecies. Cladistic and neighbor-joining analyses indicate that inferred phylogenies of mtDNA haplotypes are congruent with subspecies designations. Furthermore, in support of morphological studies, results indicate that the Mentawai macaque is most likely not a distinct species but a subspecies of M. nemestrina.
Subject(s)
DNA, Mitochondrial/genetics , Macaca nemestrina/genetics , Phylogeny , Animals , Anthropometry , Asia , Base Sequence , Genetic Variation , Humans , Molecular Sequence DataSubject(s)
Pan troglodytes/classification , Africa, Western , Animals , DNA, Mitochondrial , Humans , Pan troglodytes/genetics , PhylogenyABSTRACT
Xenopus gilli is a vulnerable anuran with a patchy distribution along the south-western coast of the Cape Province, South Africa. This species is sympatric with Xenopus laevis laevis, a widespread relative found over much of southern Africa. We examined the molecular phylogeography and population structure of the contact zone between these species to obtain information about historical biogeography and conservation management of this region. Analyses of the distribution, frequency, and cladistic and phenetic relationships among mitochondrial DNA haplotypes indicate that population subdivision is present in both taxa but that long-term isolation of sets of populations has occurred in X. gilli only. Haplotype and nucleotide diversity are also considerably higher within and among X. gilli ponds than X. l. laevis ponds in this region. We attribute the genetic segregation of X. gilli populations to ancient habitat fragmentation by ocean transgression into X. gilli habitat and to continued habitat alteration by human activity. The lower level of genetic diversity in X. L. laevis in this region is likely a result of a recent arrival of this taxon to the south-western Cape region relative to X. gilli. Population structure in X. l. laevis may be a result of isolation by distance. Clear evidence exists for at least two management units within X. gilli and strongly supports the establishment of protective measures east of False Bay in order to conserve a substantial portion of this species' extant genetic diversity.
Subject(s)
Phylogeny , Xenopus laevis/genetics , Xenopus/genetics , Animals , Base Sequence , Conservation of Natural Resources , DNA Primers/genetics , DNA, Mitochondrial/genetics , Ecosystem , Evolution, Molecular , Genetic Variation , Genetics, Population , Haplotypes , Humans , South Africa , Species SpecificityABSTRACT
Genetic variation at four microsatellite loci in conjunction with that at a highly variable allozyme locus was used to analyse paternity over a 12-year period in 13 social groups of toque macaques Macaca sinica inhabiting a natural forest in Polonnaruwa, Sri Lanka. Paternity exclusion analysis revealed that the set of offspring produced by a female usually consists of half-siblings because few males father more than one offspring with a particular female. No evidence of offspring produced by matings between first degree relatives was found. The social unit in toque macaques was not identical to the reproductive unit and the possibility of paternity by males outside the social group should be considered when estimating male reproductive output. Although it was common for multiple males to father offspring in a social group each year, reproduction within a group during a breeding season tended to be limited to a few males. The mean number of males reproducing per group per year was independent of the number of males in a group. The paternity data suggests that many males may father relatively few offspring during their entire lives and that the effective population size for toque macaques may be much smaller than indicated by demographic data.
Subject(s)
Macaca/genetics , Alleles , Animals , Animals, Wild/genetics , Animals, Wild/physiology , Dinucleotide Repeats , Female , Gene Frequency , Genetic Variation , Genetics, Population , Inbreeding , Macaca/physiology , Male , Microsatellite Repeats , Paternity , Sexual Behavior, Animal , Social Behavior , Sri LankaABSTRACT
A program simulating the distribution of variation in mitochondrial DNA in macaques is described. Empirical studies of the rates of nucleotide substitution and geographical patterning of mtDNA variation in these and other monkey species have demonstrated striking differences from equivalent measures of nuclear DNA and called into question the assumptions informing the use of mtDNA to elucidate phylogenetic relationships in organisms with relatively complex social organization. The model presented here incorporates social-structural variables as well as geographical structure and population size in order to clarify the determinants of the pattern of mtDNA evolution in macaques. The program, SHINES (Simulation of Hereditary Innovations in Neutral Evolution of Simians), employs an economical procedure for representing the haplotypes of the animals in the simulated population.
Subject(s)
Computer Simulation , DNA, Mitochondrial/genetics , Evolution, Molecular , Algorithms , Animals , Female , Founder Effect , Genetics, Population , Haplotypes , Macaca/genetics , Macaca/physiology , Macaca/psychology , Male , Mutation , Population Density , Reproduction , Social Behavior , Software , Software DesignABSTRACT
Surveys of mitochondrial DNA (mtDNA) variation in macaque monkeys have revealed extremely high levels of intraspecific divergence among haplotypes. One consistent pattern that has emerged from these studies is that divergent haplotypes are geographically segregated so that sampling a few matrilines from a given region shows them to be identical, or a closely related subset of haplotypes. Geographically structured mtDNA variation has also been commonly observed in other taxa. In this study, haplotype variation and distribution are studied in detail within a local population of toque macaques. The results show that highly divergent haplotypes, differing by 3.1% in their nucleotide sequences, coexist in this population and that they may be spatially segregated even on this micro-geographic scale. Furthermore, these differences are maintained between social groups that exchange male migrants, and thus nuclear genes, frequently.
Subject(s)
DNA, Mitochondrial/genetics , Genetic Variation/genetics , Haplotypes , Macaca/genetics , Animals , Female , Male , Restriction Mapping , Sri LankaABSTRACT
Classification of the living species of rhinoceros has been somewhat controversial. Traditionally, the two-horned rhinoceros, which includes the African (Diceros and Ceratotherium) and the Asian (Dicerorhinus) forms, has been included in one group separate from the one-horned rhinoceros (Rhinoceros). However, recently some authors have regarded the Asian species as a group separate from the African species, irrespective of the number of horns. Furthermore, others have split the living rhinoceros into three unrelated groups that include the African two-horned species in one group, the Asian two-horned rhinoceros in another group, and the Asian one-horned rhinoceros in a third group. We investigated the systematic relationships of the living rhinoceros using high-resolution restriction site mapping of the ribosomal genes of the mitochondrial DNA, and our results support the traditional subdivision of the living rhinoceros based on the number of horns. Few groups of mammals are more critically endangered than the rhinoceros, and the data obtained in this work should provide information relevant to their conservation.
Subject(s)
Perissodactyla/genetics , Animals , Base Sequence , Biological Evolution , DNA Primers/genetics , Genetic Variation/genetics , Haplotypes/genetics , Molecular Sequence Data , Phylogeny , Species SpecificityABSTRACT
Reconstructions of the human-African great ape phylogeny by using mitochondrial DNA (mtDNA) have been subject to considerable debate. One confounding factor may be the lack of data on intraspecific variation. To test this hypothesis, we examined the effect of intraspecific mtDNA diversity on the phylogenetic reconstruction of another Plio-Pleistocene radiation of higher primates, the fascicularis group of macaque (Macaca) monkey species. Fifteen endonucleases were used to identify 10 haplotypes of 40-47 restriction sites in M. mulatta, which were compared with similar data for the other members of this species group. Interpopulational, intraspecific mtDNA diversity was large (0.5%-4.5%), and estimates of divergence time and branching order incorporating this variation were substantially different from those based on single representatives of each species. We conclude that intraspecific mtDNA diversity is substantial in at least some primate species. Consequently, without prior information on the extent of genetic diversity within a particular species, intraspecific variation must be assessed and accounted for when reconstructing primate phylogenies. Further, we question the reliability of hominoid mtDNA phylogenies, based as they are on one or a few representatives of each species, in an already depauperate superfamily of primates.
Subject(s)
DNA, Mitochondrial/genetics , Macaca mulatta/genetics , Phylogeny , Animals , Asia , Genetic Variation , Hominidae/genetics , Humans , Macaca/classification , Macaca/genetics , Macaca nemestrina/genetics , Polymorphism, Genetic , Species SpecificityABSTRACT
We estimated the phylogenetic relationships of mitochondrial DNA haplotypes within the sinica-group of macaques, which includes Macaca sinica, M. radiata, M. thibetana, M. assamensis, and possibly M. arctoides. Some effort was made to detect intraspecific variation by sampling individuals from different parts of the species' range or from different matrilines. In the case of M. assamensis, individuals were sampled from both subspecies (M. assamensis assamensis and M. assamensis pelops). Total genomic DNA was extracted from blood samples and cut with a battery of 16 restriction endonucleases. A total of 97 restriction sites were mapped for these enzymes in the sinica-group and M. nemestrina, which was used as an outgroup. Phylogenetic trees constructed by both the maximum parsimony method and the neighbor-joining method were highly congruent. A bootstrap analysis of the maximum parsimony tree indicated a high degree of confidence to the association of particular haplotypes within the 80% majority rule consensus tree. An exhaustive search of all possible trees also supported this topology, although one haplotype had to be eliminated from this analysis to save computer time. The results were also unaffected by weighting the character state changes in favor of site gains over site losses. The mtDNA phylogeny produced here differs from trees based on morphology and allozymes in three ways: M. sinica and M. radiata sit in two different branches of the tree; the two subspecies of M. assamensis are separated from one another; and M. arctoides consistently fell outside the rest of the sinica-group.(ABSTRACT TRUNCATED AT 250 WORDS)
Subject(s)
DNA, Mitochondrial/genetics , Macaca/classification , Macaca/genetics , Phylogeny , Animals , Haplotypes/genetics , Models, Genetic , Restriction Mapping , Species SpecificityABSTRACT
Primates, as long-lived, iteroparous, socially complex mammals, offer the opportunity to assess the effects of behavior and demography on genetic structure. Because it is difficult to obtain tissue samples from wild primate populations, research in this area has largely been confined to terrestrial and semi-terrestrial old world monkeys (e.g., rhesus and Japanese macaques, vervets and several subspecies of baboons). However, these species display a multi-male, multi-female social structure commonly found in many other primate and non-primate mammals. Electrophoretic analyses of blood proteins from individually recognized and/or marked wild Himalayan rhesus monkeys, themselves the subject of long-term behavioral and demographic research, have begun to reveal the genetic consequences of such phenomena as social group fission, male-limited dispersion, non-consanguineous mating patterns, and agonistically defined male dominance. Specifically, rhesus social groups, consisting primarily of clusters of maternal relatives, appear to be non-random samples of a population's genotypes and genes. The genetic effects of social group fission are highly dependent on each group's size, demographic structure, and average degree of relatedness. In all cases fission contributes to the degree of intergroup genetic differentiation. Male-limited dispersion appears both to retard genetic differentiation between social groups and to lead to mating patterns that result in an avoidance of consanguinity. Groups, therefore, appear to be genetically outbred. Comparing these results with studies of other free-ranging or wild cercopithecines allows several generalizations: (a) genetic variation seems to be evenly distributed throughout each local population of multi-male social groups; (b) social groups, however, because they contain clusters of relatives, are distinctive in their specific frequencies of genes; (c) the degree of genetic differentiation between a population's social groups, because of the effects of social group fission and non-deterministic forms of male dispersal, is somewhat greater than expected on the basis of migration rates alone; and (d) the asymmetrical pattern of dispersion with respect to sex effectively precludes inbreeding in any one social group or the population as a whole. These observations have important implications for understanding the unusually rapid rates of evolution among the primates.