Continent-Wide Decoupling of Y-Chromosomal Genetic Variation from Language and Geography in Native South Americans

Numerous studies of human populations in Europe and Asia have revealed a concordance between their extant genetic structure and the prevailing regional pattern of geography and language. For native South Americans, however, such evidence has been lacking so far. Therefore, we examined the relationship between Y-chromosomal genotype on the one hand, and male geographic origin and linguistic affiliation on the other, in the largest study of South American natives to date in terms of sampled individuals and populations. A total of 1,011 individuals, representing 50 tribal populations from 81 settlements, were genotyped for up to 17 short tandem repeat (STR) markers and 16 single nucleotide polymorphisms (Y-SNPs), the latter resolving phylogenetic lineages Q and C. Virtually no structure became apparent for the extant Y-chromosomal genetic variation of South American males that could sensibly be related to their inter-tribal geographic and linguistic relationships. This continent-wide decoupling is consistent with a rapid peopling of the continent followed by long periods of isolation in small groups. Furthermore, for the first time, we identified a distinct geographical cluster of Y-SNP lineages C-M217 (C3*) in South America. Such haplotypes are virtually absent from North and Central America, but occur at high frequency in Asia. Together with the locally confined Y-STR autocorrelation observed in our study as a whole, the available data therefore suggest a late introduction of C3* into South America no more than 6,000 years ago, perhaps via coastal or trans-Pacific routes. Extensive simulations revealed that the observed lack of haplogroup C3* among extant North and Central American natives is only compatible with low levels of migration between the ancestor populations of C3* carriers and non-carriers. In summary, our data highlight the fact that a pronounced correlation between genetic and geographic/cultural structure can only be expected under very specific conditions, most of which are likely not to have been met by the ancestors of native South Americans.     

Genetic variation and population structure in native Americans

We examined genetic diversity and population structure in the American landmass using 678 autosomal microsatellite markers genotyped in 422 individuals representing 24 Native American populations sampled from North, Central, and South America. These data were analyzed jointly with similar data available in 54 other indigenous populations worldwide, including an additional five Native American groups. The Native American populations have lower genetic diversity and greater differentiation than populations from other continental regions. We observe gradients both of decreasing genetic diversity as a function of geographic distance from the Bering Strait and of decreasing genetic similarity to Siberians--signals of the southward dispersal of human populations from the northwestern tip of the Americas. We also observe evidence of: (1) a higher level of diversity and lower level of population structure in western South America compared to eastern South America, (2) a relative lack of differentiation between Mesoamerican and Andean populations, (3) a scenario in which coastal routes were easier for migrating peoples to traverse in comparison with inland routes, and (4) a partial agreement on a local scale between genetic similarity and the linguistic classification of populations. These findings offer new insights into the process of population dispersal and differentiation during the peopling of the Americas.     

Hierarchical modeling of genome‐wide Short Tandem Repeat (STR) markers infers native American prehistory

This study examines a genome‐wide dataset of 678 Short Tandem Repeat loci characterized in 444 individuals representing 29 Native American populations as well as the Tundra Netsi and Yakut populations from Siberia. Using these data, the study tests four current hypotheses regarding the hierarchical distribution of neutral genetic variation in native South American populations: (1) the western region of South America harbors more variation than the eastern region of South America, (2) Central American and western South American populations cluster exclusively, (3) populations speaking the Chibchan‐Paezan and Equatorial‐Tucanoan language stock emerge as a group within an otherwise South American clade, (4) Chibchan‐Paezan populations in Central America emerge together at the tips of the Chibchan‐Paezan cluster. This study finds that hierarchical models with the best fit place Central American populations, and populations speaking the Chibchan‐Paezan language stock, at a basal position or separated from the South American group, which is more consistent with a serial founder effect into South America than that previously described. Western (Andean) South America is found to harbor similar levels of variation as eastern (Equatorial‐Tucanoan and Ge‐Pano‐Carib) South America, which is inconsistent with an initial west coast migration into South America. Moreover, in all relevant models, the estimates of genetic diversity within geographic regions suggest a major bottleneck or founder effect occurring within the North American subcontinent, before the peopling of Central and South America. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Male lineages in South American native groups: evidence of M19 traveling south

With this study, we aimed to determine the different male ancestral components of two Native American communities from Argentina, namely Toba and Colla. The analysis of 27 Y-chromosome SNPs allowed us to identify seven different haplogroups in both samples. Chromosomes carrying the M3 mutation, which typically defines the Native American haplogroup Q1a3a, were seen most frequently in the Toba community (90%). Conversely, Q1a3a was represented in 34% of the Colla Y-chromosomes, whereas haplogroup R1b1, the main representative of western European populations, exhibited the highest frequency in this population (41%). Different M3 sublineages in the Toba community could be identified by observing point mutations at both DYS385 and M19 loci. A microvariant at DYS385, named 16.1, has been characterized, which helps to further subdivide Q1a3a. It is the first time the M19 mutated allele is described in a population from Argentina. This finding supports the old age of the lineages carrying the M19 mutation, but it contradicts the previous hypothesis that the M19 mutated allele is confined to only two Equatorial-Tucano population groups from the north region of South America. The detection of M19 further south than previously thought allows questioning of the hypothesis that this lineage serves as an example of isolation after colonization. This observation also affirms the strong genetic drift to which Native Americans have been subjected. Moreover, our study illustrates a heterogeneous contribution of Europeans to these populations and supports previous studies showing that most Native American groups were subjected to European admixture that primarily involved immigrant men.     

Remarkable karyotypic homogeneity in a widespread tropical fish species: Hoplosternum littorale (Siluriformes, Callichthyidae)

The first chromosomal data in Hoplosternum littorale from an isolated South American drainage in north-eastern Brazil are presented. All specimens were characterized by a diploid number (2n) of 60 chromosomes divided into three metacentric, one submetacentric and 26 acrocentric pairs; single nucleolar organizer regions (NOR) on the sixth pair; centromeric and interstitial heterochromatin; GC-rich sites on four large acrocentric chromosomes, including the NOR-bearing pair, and 5S ribosomal genes at terminal region on short arms of two acrocentric pairs. These data are invariably similar to previous reports in H. littorale from distant localities throughout South America, which contrasts with the chromosomal diversity of Callichthyidae and reinforces the role of human activities on the dispersal and colonization of this fish.     

A new topology of the human Y chromosome haplogroup E1b1 (E-P2) revealed through the use of newly characterized binary polymorphisms

Haplogroup E1b1, defined by the marker P2, is the most represented human Y chromosome haplogroup in Africa. A phylogenetic tree showing the internal structure of this haplogroup was published in 2008. A high degree of internal diversity characterizes this haplogroup, as well as the presence of a set of chromosomes undefined on the basis of a derived character. Here we make an effort to update the phylogeny of this highly diverse haplogroup by including seven mutations which have been newly discovered by direct resequencing. We also try to incorporate five previously-described markers which were not, however, reported in the 2008 tree. Additionally, during the process of mapping, we found that two previously reported SNPs required a new position on the tree. There are three key changes compared to the 2008 phylogeny. Firstly, haplogroup E-M2 (former E1b1a) and haplogroup E-M329 (former E1b1c) are now united by the mutations V38 and V100, reducing the number of E1b1 basal branches to two. The new topology of the tree has important implications concerning the origin of haplogroup E1b1. Secondly, within E1b1b1 (E-M35), two haplogroups (E-V68 and E-V257) show similar phylogenetic and geographic structure, pointing to a genetic bridge between southern European and northern African Y chromosomes. Thirdly, most of the E1b1b1* (E-M35*) paragroup chromosomes are now marked by defining mutations, thus increasing the discriminative power of the haplogroup for use in human evolution and forensics.     

On the origins and genetic diversity of South American chickens: one step closer

Local chicken populations are a major source of food in the rural areas of South America. However, very little is known about their genetic composition and diversity. Here, we analyzed five populations from South America to investigate their maternal genetic origin and diversity, hoping to mitigate the lack of information on local chicken populations from this region. We also included three populations of chicken from the Iberian Peninsula and one from Easter Island, which are potential sources of the first chickens introduced in South America. The obtained sequencing data from South American chickens indicate the presence of four haplogroups (A, B, E and D) that can be further subdivided into nine sub‐haplogroups. Of these, four (B1, D1a, E1a(b), E1b) were absent from local Iberian Peninsula chickens and one (D1a) was present only on Easter Island. The presence of the sub‐haplogroups A1a(b) and E1a(b) in South America, previously only observed in Eastern Asia, and the significant population differentiation between Iberian Peninsula and South American populations, suggest a second maternal source of the extant genetic pool in South American chickens.     

Biological relationship between Central and South American Chibchan speaking populations: evidence from mtDNA

We examined mitochondrial DNA (mtDNA) haplogroup and haplotype diversity in 188 individuals from three Chibchan (Kogi, Arsario, and Ijka) populations and one Arawak (Wayuú) group from northeast Colombia to determine the biological relationship between lower Central American and northern South American Chibchan speakers. mtDNA haplogroups were obtained for all individuals and mtDNA HVS-I sequence data were obtained for 110 samples. Resulting sequence data were compared to 16 other Caribbean, South, and Central American populations using diversity measures, neutrality test statistics, sudden and spatial mismatch models, intermatch distributions, phylogenetic networks, and a multidimensional scaling plot. Our results demonstrate the existence of a shared maternal genetic structure between Central American Chibchan, Mayan populations and northern South American Chibchan-speakers. Additionally, these results suggest an expansion of Chibchan-speakers into South America associated with a shift in subsistence strategies because of changing ecological conditions that occurred in the region between 10,000-14,000 years before present.     

Relationships among cave swallow populations (Petrochelidon fulva) determined by comparisons of microsatellite and cytochrome b data

The cave swallow (Petrochelidon fulva) is a polytypic species with isolated populations in northwestern South America, southwestern North America, Yucatan, Greater Antilles, and Florida. We compared microsatellite genotypes of at least five individuals each from five populations and cytochrome b sequence data of two individuals each from seven populations plus two outgroups. Microsatellite allelic diversity was substantial, and the North American populations were about equally variable. In contrast, the Ecuadorian population had far less genetic variation. Gene flow was apparent among populations, especially between Texas and Florida. Genetic structure was greater than in widespread North American species but less than that of sedentary Neotropical birds. Microsatellite genetic distances indicated a close affinity between Ecuadorian and northern populations, especially Texas and Florida, but this finding was inconsistent with cytochrome b data, which indicated that the Ecuadorian population is the clear outgroup to the northern populations. Its outgroup status is consistent with recent classifications that designate South American populations as their own species (P. rufocollaris). The cytochrome b data further suggested that the northern populations are divided into two clades: Texas/Yucatan and Florida/Greater Antilles. The microsatellite data incorrectly measured the diversity and affinities of Ecuadorian birds apparently because of an ascertainment bias that results from the use of heterologous PCR primers. Despite these problems in measuring phylogenetic relationships, the microsatellite data appeared to work well as a population genetic marker in indicating population structure and gene flow.     

Phylogenetic position of South American Cheilanthes (Cheilanthoideae,Pteridaceae): Advances in the generic circumscription and segregation of the new genus Mineirella

This analysis corroborates and expands our previous results regarding the phylogenetic position of Cheilanthes species from South America. We sequenced three plastid genetic regions, one genic (rbcL) and two genic plus intergenic spacers (trnL + trnL-F and rps4 + rps4-trnS) from 25 South American cheilanthoid species. This allowed us to elucidate phylogenetic relationships that have been historically unresolved or were lowly supported. Here, we analyzed 45 Cheilanthes species (23 from South America) and circumscribed Cheilanthes s.s. in a strongly supported clade that contains three subclades: (i) exclusively from South America, (ii) from Australasia + South America, and (iii) from Africa. The position of three South American species, previously referred to the informal “Cheilanthes geraniifolia group”, is confirmed as a highly supported group outside Cheilanthes s.s. and within the Adiantopsis–Doryopteris clade. This group is described here as the new genus Mineirella. The new combinations for the genus and illustrations are included. Additionally, we discuss the morphological innovations that provide evidence to support the different clades.     

Autosomal, mtDNA, and Y-chromosome diversity in Amerinds: pre- and post-Columbian patterns of gene flow in South America

To evaluate sex-specific differences in gene flow between Native American populations from South America and between those populations and recent immigrants to the New World, we examined the genetic diversity at uni- and biparental genetic markers of five Native American populations from Colombia and in published surveys from native South Americans. The Colombian populations were typed for five polymorphisms in mtDNA, five restriction sites in the beta-globin gene cluster, the DQA1 gene, and nine autosomal microsatellites. Elsewhere, we published results for seven Y-chromosome microsatellites in the same populations. Autosomal polymorphisms showed a mean G(ST) of 6.8%, in agreement with extensive classical marker studies of South American populations. MtDNA and Y-chromosome markers resulted in G(ST) values of 0.18 and 0.165, respectively. When only Y chromosomes of confirmed Amerind origin were used in the calculations (as defined by the presence of allele T at locus DYS199), G(ST) increased to 0.22. G(ST) values calculated from published data for other South American natives were 0.3 and 0.29 for mtDNA and Amerind Y chromosomes, respectively. The concordance of these estimates does not support an important difference in migration rates between the sexes throughout the history of South Amerinds. Admixture analysis of the Colombian populations suggests an asymmetric pattern of mating involving mostly immigrant men and native women.     

Genetic structure of Quechua-speakers of the Central Andes and geographic patterns of gene frequencies in South Amerindian populations

A sample of 141 Quechua-speaking individuals of the population of Tayacaja, in the Peruvian Central Andes, was typed for the following 16 genetic systems: ABO, Rh, MNSs, P, Duffy, AcP1, EsD, GLOI, PGM1, AK, 6-PGD, Hp, Gc, Pi, C3, and Bf. The genetic structure of the population was analyzed in relation to the allele frequencies available for other South Amerindian populations, using a combination of multivariate and multivariable techniques. Spatial autocorrelation analysis was performed independently for 13 alleles to identify patterns of gene flow in South America as a whole and in more specific geographic regions. We found a longitudinal cline for the AcP1*a and EsD*1 alleles which we interpreted as the result of an ancient longitudinal expansion of a putative ancestral population of modern Amerindians. Monmonnier's algorithm, used to identify areas of sharp genetic discontinuity, suggested a clear east-west differentiation of native South American populations, which was confirmed by analysis of the distribution of genetic distances. We suggest that this pattern of genetic structures is the consequence of the independent peopling of western and eastern South America or to low levels of gene flow between these regions, related to different environmental and demographic histories.     

Phylogeny of the large extinct South American Canids (Mammalia,Carnivora, Canidae) using a “total evidence” approach

South America currently possesses a high diversity of canids, comprising mainly small to medium‐sized omnivorous species, but in the Pleistocene there were large hypercarnivorous taxa that were assigned to Protocyon spp., Theriodictis spp., Canis gezi, Canis nehringi and Canis dirus. These fossils have never been included in phylogenies based on quantitative cladistics, but hand‐constructed cladograms published in the 1980s included some of them in the South American canine clade and others in the Canis clade. In this work, the phylogenetic position of the large extinct South American canids was studied using a large sample of living and extinct canids, as well as different sources of characters (e.g. DNA and 133 osteological characters). The phylogenetic analysis corroborates the inclusion of Theriodictis and Protocyon in the “South American clade”, where C. gezi is also included. In addition, the position of C. dirus as a highly derived Canis species is confirmed. The simultaneous analysis supports hypercarnivory having arisen at least three times in Caninae and once in the “South American clade”. The combination of the phylogenetic analyses, the fossil record and divergence dates estimated in previous works suggests that at least three or four independent lineages of the “South American clade” invaded South America after the establishment of the Panama bridge around 3 million years ago, plus other events corresponding to the immigration of Urocyon and Canis dirus.
© The Willi Hennig Society 2009.     

Phylogeography of the bushmaster (Lachesis tnuta: Viperidae): implications for neotropical biogeography, systematics, and conservation

We used mitochondrial gene sequences to reconstruct phylogenetic relationships among subspecies of the bushmaster, Lachesis muta. These large vipers are widely distributed in lowland tropical forests in Central and South America, where three of four allopatric subspecies are separated by montane barriers. Our phylogeny indicates that the four subspecies belong to two clades, the Central American and South American lineages. We use published molecular studies of other taxa to estimate a 'reptilian mtDNA rate' and thus temporal boundaries for major lineage divergences in Lachesis. We estimate that the Central and South American forms diverged 18-6 Mya, perhaps due to the uplifting of the Andes, whereas the two Central American subspecies may have diverged 11-4 Mya with the uprising of the Cordillera de Talamanca that separates them today. South American bushmasters from the Amazon Basin and the Atlantic Forest are not strongly differentiated, perhaps due to episodic gene flow during the Pleistocene, when suitable habitat for this species was at times more continuous. Our results agree with previous evidence that genetic divergence among some neotropical vertebrates pre-dated Pleistocene forest fragmentation cycles and the appearance of the Panamanian Isthmus. Based on morphological, behavioral, and molecular evidence, we recognize three species of Lachesis. In addition to L. muta, the widespread South American form, the Central American forms are treated as distinct species (L. meknocephak and L. stenophrys), each deserving of special conservation status due to restricted distribution and habitat destruction.     

Mitochondrial DNA and the peopling of South America

The initial peopling of South America is largely unresolved, in part because of the unique distribution of genetic diversity in native South Americans. On average, genetic diversity estimated within Andean populations is higher than that estimated within Amazonian populations. Yet there is less genetic differentiation estimated among Andean populations than estimated among Amazonian populations. One hypothesis is that this pattern is a product of independent migrations of genetically differentiated people into South America. A competing hypothesis is that there was a single migration followed by regional isolation. In this study we address these hypotheses using mtDNA hypervariable region 1 sequences representing 21 South American groups and include new data sets for four native Peruvian communities from Tupe, Yungay, and Puno. An analysis of variance that compared the combined data from western South America to the combined data from eastern South America determined that these two regional data sets are not significantly different. As a result, a migration from a single source population into South America serves as the simplest explanation of the data.     

Molecular systematics and paleobiogeography of the South American sigmodontine rodents [published erratum appears in Mol Biol Evol 1998 Feb;15(2):224]

The murid rodent subfamily Sigmodontinae contains 79 genera which are distributed throughout the New World. The time of arrival of the first sigmodontines in South America and the estimated divergence time(s) of the different lineages of South American sigmodontines have been controversial due to the lack of a good fossil record and the immense number of extant species. The "early-arrival hypothesis" states that the sigmodontines must have arrived in South America no later than the early Miocene, at least 20 MYA, in order to account for their vast present-day diversity, whereas the "late-arrival hypothesis" includes the sigmodontines as part of the Plio-Pleistocene Great American Interchange, which occurred approximately 3.5 MYA. The phylogenetic relationships among 33 of these genera were reconstructed using mitochondrial DNA (mtDNA) sequence data from the ND3, ND4L, arginine tRNA, and ND4 genes, which we show to be evolving at the same rate. A molecular clock was calibrated for these genes using published fossil dates, and the genetic distances were estimated from the DNA sequences in this study. The molecular clock was used to estimate the dates of the South American sigmodontine origin and the main sigmodontine radiation in order to evaluate the "early-" and "late-arrival" scenarios. We estimate the time of the sigmodontine invasion of South America as between approximately 5 and 9 MYA, supporting neither of the scenarios but suggesting two possible models in which the invading lineage was either (1) ancestral to the oryzomyines, akodonts, and phyllotines or (2) ancestral to the akodonts and phyllotines and accompanied by the oryzomyines. The sigmodontine invasion of South America provides an example of the advantage afforded to a lineage by the fortuitous invasion of a previously unexploited habitat, in this case an entire continent.      

Genetic Diversity of Neotropical Myotis (Chiroptera: Vespertilionidae) with an Emphasis on South American Species

Background

Cryptic morphological variation in the Chiropteran genus Myotis limits the understanding of species boundaries and species richness within the genus. Several authors have suggested that it is likely there are unrecognized species-level lineages of Myotis in the Neotropics. This study provides an assessment of the diversity in New World Myotis by analyzing cytochrome-b gene variation from an expansive sample ranging throughout North, Central, and South America. We provide baseline genetic data for researchers investigating phylogeographic and phylogenetic patterns of Myotis in these regions, with an emphasis on South America.

Methodology and Principal Findings

Cytochrome-b sequences were generated and phylogenetically analyzed from 215 specimens, providing DNA sequence data for the most species of New World Myotis to date. Based on genetic data in our sample, and on comparisons with available DNA sequence data from GenBank, we estimate the number of species-level genetic lineages in South America alone to be at least 18, rather than the 15 species currently recognized.

Conclusions

Our findings provide evidence that the perception of lower species richness in South American Myotis is largely due to a combination of cryptic morphological variation and insufficient sampling coverage in genetic-based systematic studies. A more accurate assessment of the level of diversity and species richness in New World Myotis is not only helpful for delimiting species boundaries, but also for understanding evolutionary processes within this globally distributed bat genus.     

Sudden-death syndrome of soybean is caused by two morphologically and phylogenetically distinct species within the Fusarium solani species complex--F. virguliforme in North America and F. tucumaniae in South America

Soybean sudden-death syndrome has become a serious constraint to commercial production of this crop in North and South America during the past decade. To assess whether the primary etiological agent is panmictic in both hemispheres, morphological and molecular phylogenetic analyses were conducted on strains selected to represent the known pathogenic and genetic diversity of this pathogen. Maximum-parsimony analysis of DNA sequences from the nuclear ribosomal intergenic spacer region and the single copy nuclear gene translation elongation factor 1-α, together with detailed morphological comparisons of conidial features, indicate that SDS of soybean in North and South America is caused by two phylogenetically and morphologically distinct species. Fusarium virguliforme sp. nov., formally known as F. solani f. sp. glycines, is described and illustrated for the SDS pathogen in North America, and F. tucumaniae sp. nov. is proposed for the South American pathogen. The molecular phylogenetic results challenge the forma specialis naming system because pathogenicity to soybean might have evolved convergently in F. tucumaniae and F. virguliforme. Phylogenetic evidence indicates the two SDS pathogens do not share a most recent common ancestor, since F. tucumaniae was resolved as a sister to a pathogen of Phaseolus vulgaris, F. phaseoli comb. nov. All three pathogens appear to have evolutionary origins in the southern hemisphere since they are deeply nested within a South American clade of the F. solani species complex.     

The Great American Interchange in birds: a phylogenetic perspective with the genus Trogon

The 'Great American Interchange' (GAI) is recognized as having had a dramatic effect on biodiversity throughout the Neotropics. However, investigation of patterns in Neotropical avian biodiversity has generally been focused on South American taxa in the Amazon Basin, leaving the contribution of Central American taxa under-studied. More rigorous studies of lineages distributed across the entire Neotropics are needed to uncover phylogeographical patterns throughout the area, offering insights into mechanisms that contribute to overall Neotropical biodiversity. Here we use mitochondrial DNA sequence data and intensive geographical sampling from the widespread Neotropical avian genus Trogon to investigate the role of the GAI in shaping its phylogeographical history. Our results show that genetic diversity in Trogon exceeds the perceived biodiversity, and that the GAI resulted in lineage diversification within the genus. Despite greater diversity in South America, a Central American centre of origin with multiple and independent dispersals into South America is indicated. These dispersals were followed by the evolution of divergent lineages associated with the Andes Mountains and other South American geographical features. According to our phylogenetic reconstructions, several species, which were originally defined by morphological characters, are nonmonophyletic. In sum, our results elucidate the evolutionary history of Trogon , reveal patterns obscured by extant biodiversity, and serve as a biogeographical model to consider in future studies.