Population structure among African and derived populations of Drosophila simulans: evidence for ancient subdivision and recent admixture.

Previous studies based on allozyme variation have found little evidence for genetic differentiation in Drosophila simulans. On the basis of DNA sequence variation at two nuclear loci in four African populations of D. simulans, we show that there is significant structure to D. simulans populations within Africa. Variation at one of the loci, vermilion, appears to be neutral and supports an eastern African origin for European and American populations. Samples from the West Indies, Europe, and North America had a nucleotide diversity lower than that of African populations at vermilion and show nonequilibrium haplotype distributions at both vermilion and G6pd, consistent with a hypothesis of recent bottleneck and possibly also admixture in the history of these populations. Directional selection, previously documented at G6pd, appears to have occurred within the coalescence time of the species, obscuring deep population history.     

Microsatellite variation and differentiation in African and non-African populations of Drosophila simulans

Drosophila simulans originated in sub-Saharan Africa or Madagascar and colonized the rest of the world after the last glaciation about 10 000 years ago. Consistent with this demographic history, sub-Saharan African populations have been shown to harbour higher levels of microsatellite and sequence variation than cosmopolitan populations. Nevertheless, only limited information is available on the population structure of D. simulans. Here, we analysed X-linked and autosomal microsatellite loci in four sub-Saharan African, one North African, one Israeli, and two European D. simulans populations. Bayesian clustering algorithms combined the North African, Israeli, and European populations into a single cosmopolitan group. The four sub-Saharan populations were split into two separate groups. Pairwise F(ST) analysis, however, indicated significant population differentiation between all eight populations surveyed. A significant signal for population reduction in cosmopolitan populations was found only for X-linked loci.     

Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans

Surveys of molecular variation in Drosophila melanogaster and Drosophila simulans have suggested that diversity outside of Africa is a subset of that within Africa. It has been argued that reduced levels of diversity in non-African populations reflect a population bottleneck, adaptation to temperate climates, or both. Here, I summarize the available single-nucleotide polymorphism data for both species. A simple "out of Africa" bottleneck scenario is consistent with geographic patterns for loci on the X chromosome but not with loci on the autosomes. Interestingly, there is a trend toward lower nucleotide diversity on the X chromosome relative to autosomes in non-African populations of D. melanogaster, but the opposite trend is seen in African populations. In African populations, autosomal inversion polymorphisms in D. melanogaster may contribute to reduced autosome diversity relative to the X chromosome. To elucidate the role that selection might play in shaping patterns of variability, I present a summary of within- and between-species patterns of synonymous and replacement variation in both species. Overall, D. melanogaster autosomes harbor an excess of amino acid replacement polymorphisms relative to D. simulans. Interestingly, range expansion from Africa appears to have had little effect on synonymous-to-replacement polymorphism ratios.     

Contrasted polymorphism patterns in a large sample of populations from the evolutionary genetics model Drosophila simulans

African populations of Drosophila simulans are thought to be ancestral in this model species and are increasingly used for testing general hypotheses in evolutionary genetics. It is often assumed that African populations are more likely to be at a neutral mutation drift equilibrium than other populations. Here we examine population structuring and the demographic profile in nine populations of D. simulans. We surveyed sequence variation in four X-linked genes (runt, sevenless, Sex-lethal, and vermilion) that have been used in a parallel study in the closely related species D. melanogaster. We found that an eastern group of populations from continental Africa and Indian Ocean islands (Kenya, Tanzania, Madagascar, and Mayotte Island) is widespread, shows little differentiation, and has probably undergone demographic expansion. The other two African populations surveyed (Cameroon and Zimbabwe) show no evidence of population expansion and are markedly differentiated from each other as well as from the populations from the eastern group. Two other populations, Europe and Antilles, are probably recent invaders to these areas. The Antilles population is probably derived from Europe through a substantial bottleneck. The history of these populations should be taken into account when drawing general conclusions from variation patterns.     

Genetic variation and differentiation at microsatellite loci in Drosophila simulans. Evidence for founder effects in new world populations.

Drosophila simulans isofemale lines from Africa, South America, and two locations in North America were surveyed for variation at 16 microsatellite loci on the X, second, and third chromosomes, and 18 microsatellites, which are unmapped. D. simulans is thought to have colonized New World habitats only relatively recently (within the last few hundred years). Consistent with a founder effect occurring as colonizers moved into these New World habitats, we find less microsatellite variability in North and South American D. simulans populations than for an African population. Population subdivision as measured at microsatellites is moderate when averaged across all loci (FST = 0.136), but contrasts sharply with previous studies of allozyme variation, which have showed significantly less differentiation in D. simulans than in D. melanogaster. There are substantially fewer private alleles observed in New World populations of D. simulans than seen in a similar survey of D. melanogaster. In addition to possible differences in population size during their evolutionary histories, varying colonization histories or other demographic events may be necessary to explain discrepancies in the patterns of variation observed at various genetic markers between these closely related species.     

Historicity and the Population Genetics of Drosophila Melanogaster and D. Simulans

We summarize data showing that there is population structure in African populations of Drosophila from the melanogaster-simulans complex. In D. melanogaster, population structuring is found at individual loci, but is obscured by population structuring for large inversions that simultaneously affect several loci. In D. simulans, molecular polymorphism at the X-linked vermilion locus suggests that different groups of populations have been geographically isolated for some time. Invading populations are probably derived from different areas in Africa. European populations originate from an east African population that was probably not at a demographic equilibrium. The origin of the Antilles population is apparently different and is as yet unknown. In south-western France, populations from these two species undergo different population structuring at the scale of a few kilometres: D. melanogaster makes up a large panmictic population, whereas D. simulans forms a metapopulation that is divided into smaller demes.     

The Paternal Landscape along the Bight of Benin – Testing Regional Representativeness of West-African Population Samples Using Y-Chromosomal Markers

Patterns of genetic variation in human populations across the African continent are still not well studied in comparison with Eurasia and America, despite the high genetic and cultural diversity among African populations. In population and forensic genetic studies a single sample is often used to represent a complete African region. In such a scenario, inappropriate sampling strategies and/or the use of local, isolated populations may bias interpretations and pose questions of representativeness at a macrogeographic-scale. The non-recombining region of the Y-chromosome (NRY) has great potential to reveal the regional representation of a sample due to its powerful phylogeographic information content. An area poorly characterized for Y-chromosomal data is the West-African region along the Bight of Benin, despite its important history in the trans-Atlantic slave trade and its large number of ethnic groups, languages and lifestyles. In this study, Y-chromosomal haplotypes from four Beninese populations were determined and a global meta-analysis with available Y-SNP and Y-STR data from populations along the Bight of Benin and surrounding areas was performed. A thorough methodology was developed allowing comparison of population samples using Y-chromosomal lineage data based on different Y-SNP panels and phylogenies. Geographic proximity turned out to be the best predictor of genetic affinity between populations along the Bight of Benin. Nevertheless, based on Y-chromosomal data from the literature two population samples differed strongly from others from the same or neighbouring areas and are not regionally representative within large-scale studies. Furthermore, the analysis of the HapMap sample YRI of a Yoruban population from South-western Nigeria based on Y-SNPs and Y-STR data showed for the first time its regional representativeness, a result which is important for standard population and forensic genetic applications using the YRI sample. Therefore, the uniquely and powerful geographical information carried by the Y-chromosome makes it an important locus to test the representativeness of a certain sample even in the genomic era, especially in poorly investigated areas like Africa.     

Isolation of Y chromosome-specific microsatellites in the horse and cross-species amplification in the genus Equus

Y chromosome polymorphisms such as microsatellites or single nucleotide polymorphisms represent a paternal counterpart to mitochondrial DNA (mtDNA) for evolutionary and phylogeographic studies. The use of Y chromosome haplotyping in natural populations of species other than humans is still hindered by the lack of sequence information necessary for polymorphism screening. Here we used representational difference analysis (RDA) followed by a screen of a bacterial artificial chromosome (BAC) library for repetitive sequences to obtain polymorphic Y-chromosomal markers. The procedure was performed for the domestic horse (Equus caballus) and we report the first six Y-chromosomal microsatellite markers for this species. Three markers were also useful for haplotyping taxa of the zebra/ass lineage. Y-chromosomal microsatellite markers show a single haplotype in the domestic horse, whereas notable variation has been observed in the other members of the genus Equus.     

African Drosophila melanogaster and D. simulans populations have similar levels of sequence variability, suggesting comparable effective population sizes

Drosophila melanogaster and D. simulans are two closely related species with a similar distribution range. Many studies suggested that D. melanogaster has a smaller effective population size than D. simulans. As most evidence was derived from non-African populations, we readdressed this question by sequencing 10 X-linked loci in five African D. simulans and six African D. melanogaster populations. Contrary to previous results, we found no evidence for higher variability, and thus larger effective population size, in D. simulans. Our observation of similar levels of variability of both species will have important implications for the interpretation of patterns of molecular evolution.     

Worldwide distribution of transposable element copy number in natural populations of Drosophila simulans

Abstract.— Transposable elements (TEs), which promote various kinds of mutations, constitute a large fraction of the genome. How they invade natural populations and species is therefore of fundamental importance for understanding the dynamics of genetic diversity and genome composition. On the basis of 85 samples of natural populations of Drosophila simulans , we report the distributions of the genome insertion site numbers of nine TEs that were chosen because they have a low average number of sites. Most populations were found to have 0–3 insertion sites, but some of them had a significantly higher number of sites for a given TE. The populations located in regions outside Africa had the highest number of sites for all elements except HMS Beagle and Coral , suggesting a recent increase in the activity of some TEs associated with the colonization patterns of Drosophila simulans . The element Tirant had a very distinctive pattern of distribution: it was identified mainly in populations from East Africa and some islands in the Indian Ocean, and its insertion site number was low in all these populations. The data suggest that the genome of the entire species of Drosophila simulans may be being invaded by TEs from populations in which they are present in high copy number.     

Molecular Variation at the Vermilion Locus in Geographically Diverse Populations of Drosophila Melanogaster and D. Simulans

We surveyed nucleotide variation at vermilion in population samples of Drosophila melanogaster from Africa, Asia and the Americas to test the hypothesis that the vermilion gene was a target of balancing selection and to improve our understanding of geographic differentiation. Patterns of polymorphism and divergence showed no evidence for non-neutral evolution. However, the frequency spectrum of polymorphic sites in some non-African samples departed from the neutral equilibrium expectation. Furthermore, there were high levels of linkage disequilibrium in non-African samples, despite apparently high rates of crossing over in the vermilion region. In the absence of comparable data from other loci in these same population samples, we cannot determine whether the unusual patterns of variation at vermilion reflect demographic as opposed to locus-specific events. We found surprisingly high levels of differentiation at vermilion between U.S. and Congo samples of D. simulans. In light of previously published allozyme and mtDNA data that provided no evidence for significant differentiation between African and non-African D. simulans populations, the vermilion data raise the possibility that both mtDNA and allozymes have been influenced by selection.     

History of click-speaking populations of Africa inferred from mtDNA and Y chromosome genetic variation

Little is known about the history of click-speaking populations in Africa. Prior genetic studies revealed that the click-speaking Hadza of eastern Africa are as distantly related to click speakers of southern Africa as are most other African populations. The Sandawe, who currently live within 150 km of the Hadza, are the only other population in eastern Africa whose language has been classified as part of the Khoisan language family. Linguists disagree on whether there is any detectable relationship between the Hadza and Sandawe click languages. We characterized both mtDNA and Y chromosome variation of the Sandawe, Hadza, and neighboring Tanzanian populations. New genetic data show that the Sandawe and southern African click speakers share rare mtDNA and Y chromosome haplogroups; however, common ancestry of the 2 populations dates back >35,000 years. These data also indicate that common ancestry of the Hadza and Sandawe populations dates back >15,000 years. These findings suggest that at the time of the spread of agriculture and pastoralism, the click-speaking populations were already isolated from one another and are consistent with relatively deep linguistic divergence among the respective click languages.     

Characterization of non-cytoplasmic incompatibility inducing Wolbachia in two continental African populations of Drosophila simulans

Wolbachia is an endocellular bacterium infecting arthropods and nematodes. In arthropods, it invades host populations through various mechanisms, affecting host reproduction, the most common of which being cytoplasmic incompatibility (CI). CI is an embryonic mortality occurring when infected males mate with uninfected females or females infected by a different Wolbachia strain. This phenomenon is observed in Drosophila simulans, an intensively studied Wolbachia host, harbouring at least five distinct bacterial strains. In this study, we investigate various aspects of the Wolbachia infections occurring in two continental African populations of D. simulans: CI phenotype, phylogenetic position based on the wsp gene and associated mitochondrial haplotype. From the East African population (Tanzania), we show that (i) the siIII mitochondrial haplotype occurs in continental populations, which was unexpected based on the current views of D. simulans biogeography, (ii) the wKi strain (that rescues from CI while being unable to induce it) is very closely related to the CI-inducing strain wNo, (iii) wKi and wNo might not derive from a unique infection event, and (iv) wKi is likely to represent the same entity as the previously described wMa variant. In the West African population (Cameroon), the Wolbachia infection was found identical to the previously described wAu, which does not induce CI. This finding supports the view that wAu might be an ancient infection in D. simulans.     

A predominantly neolithic origin for Y-chromosomal DNA variation in North Africa

We have typed 275 men from five populations in Algeria, Tunisia, and Egypt with a set of 119 binary markers and 15 microsatellites from the Y chromosome, and we have analyzed the results together with published data from Moroccan populations. North African Y-chromosomal diversity is geographically structured and fits the pattern expected under an isolation-by-distance model. Autocorrelation analyses reveal an east-west cline of genetic variation that extends into the Middle East and is compatible with a hypothesis of demic expansion. This expansion must have involved relatively small numbers of Y chromosomes to account for the reduction in gene diversity towards the West that accompanied the frequency increase of Y haplogroup E3b2, but gene flow must have been maintained to explain the observed pattern of isolation-by-distance. Since the estimates of the times to the most recent common ancestor (TMRCAs) of the most common haplogroups are quite recent, we suggest that the North African pattern of Y-chromosomal variation is largely of Neolithic origin. Thus, we propose that the Neolithic transition in this part of the world was accompanied by demic diffusion of Afro-Asiatic-speaking pastoralists from the Middle East.     

Phylogeography of the African buffalo based on mitochondrial and Y-chromosomal loci: Pleistocene origin and population expansion of the Cape buffalo subspecies

Population genetics and phylogeography of the African buffalo (Syncerus caffer) are inferred from genetic diversity at mitochondrial D-loop hypervariable region I sequences and a Y-chromosomal microsatellite. Three buffalo subspecies from different parts of Africa are included. Nucleotide diversity of the subspecies Cape buffalo at hypervariable region I is high, with little differentiation between populations. A mutation rate of 13-18% substitutions/million years is estimated for hypervariable region I. The nucleotide diversity indicates an estimated female effective population size of 17 000-32 000 individuals. Both mitochondrial and Y-chromosomal diversity are considerably higher in buffalo from central and southwestern Africa than in Cape buffalo, for which several explanations are hypothesized. There are several indications that there was a late middle to late Pleistocene population expansion in Cape buffalo. This also seems to be the period in which Cape buffalo evolved as a separate subspecies, according to the net sequence divergence with the other subspecies. These two observations are in agreement with the hypothesis of a rapid evolution of Cape buffalo based on fossil data. Additionally, there appears to have been a population expansion from eastern to southern Africa, which may be related to vegetation changes. However, as alternative explanations are also possible, further analyses with autosomal loci are needed.     

Patterns of microsatellite variability among X chromosomes and autosomes indicate a high frequency of beneficial mutations in non-African D. simulans

We analyzed microsatellite variability at 42 X-linked and 39 autosomal loci from African and European populations of Drosophila simulans. The African D. simulans harbored significantly more microsatellite variability than the European flies. In the European population, X-linked polymorphism was more reduced than autosomal variation, whereas there was no significant difference between chromosomes in the African population. Previous studies also observed a similar pattern but failed to distinguish between a demographic event and a selection scenario. We performed extensive computer simulations using a wide range of demographic scenarios to distinguish between the two hypotheses. Approximate summary likelihood estimates differed dramatically among X chromosomes and autosomes. Furthermore, our experimental data showed a surplus of X-linked microsatellites with a significantly reduced variability in non-African D. simulans. We conclude that our data are not compatible with a neutral scenario. Thus, the reduced variability at X-linked loci is most likely caused by selective sweeps associated with the out-of-Africa habitat expansion of D. simulans.     

The Y chromosomes of Drosophila simulans are highly polymorphic for their ability to suppress sex-ratio drive

The sex-ratio trait, known in several species of Drosophila including D. simulans, results from meiotic drive of the X chromosome against the Y. Males that carry a sex-ratio X chromosome produce strongly female-biased progeny. In D. simulans, drive suppressors have evolved on the Y chromosome and on the autosomes. Both the frequency of sex-ratio X and the strength of the total drive suppression (Y-linked and autosomal) vary widely among geographic populations of this worldwide species. We have investigated the pattern of Y-linked drive suppression in six natural populations representative of this variability. Y-linked suppressors were found to be a regular component of the suppression, with large differences between populations in the mean level of suppression. These variations did not correspond to differences in frequency of discrete types of Y chromosomes, but to a more or less wide continuum of phenotypes, from nonsuppressor to partial or total suppressor. We concluded that a large diversity of Y-linked suppressor alleles exists in D. simulans and that some populations are highly polymorphic. Our results support the hypothesis that a Y-chromosome polymorphism can be easily maintained by a balance between meiotic drive and the cost of drive suppression.     

Influence of two Wolbachia strains on population structure of East African Drosophila simulans

Drosophila simulans is hypothesized to have originated in continental East Africa or Madagascar. In this study, we investigated evolutionary forces operating on mitochondrial DNA (mtDNA) in populations of D. simulans from Zimbabwe, Malawi, Tanzania, and Kenya. Variation in mtDNA may be affected by positive selection, background selection, demographic history, and/or any maternally inherited factor such as the bacterial symbiont Wolbachia. In East Africa, the wRi and wMa Wolbachia strains associate with the siII or siIII mitochondrial haplogroups, respectively. To ask how polymorphism relates to Wolbachia infection status, we sequenced 1776 bp of mitochondrial DNA and 1029 bp of the X-linked per locus from 79 lines. The two southern populations were infected with wRi and exhibited significantly reduced mtDNA variation, while Wolbachia-uninfected siII flies from Tanzania and Kenya showed high levels of mtDNA polymorphism. These are the first known populations of D. simulans that do not exhibit reduced mtDNA variation. We observed no mitochondrial variation in the siIII haplogroup regardless of Wolbachia infection status, suggesting positive or background selection. These populations offer a unique opportunity to monitor evolutionary dynamics in ancestral populations that harbor multiple strains of Wolbachia.     

The Genetic Basis of Haldane''s Rule and the Nature of Asymmetric Hybrid Male Sterility among Drosophila Simulans, Drosophila Mauritiana and Drosophila Sechellia

Haldane's rule (i.e., the preferential hybrid sterility and inviability of heterogametic sex) has been known for 70 years, but its genetic basis, which is crucial to the understanding of the process of species formation, remains unclear. In the present study, we have investigated the genetic basis of hybrid male sterility using Drosophila simulans, Drosophila mauritiana and Drosophila sechellia. An introgression of D. sechellia Y chromosome into a fairly homogenous background of D. simulans did not show any effect of the introgressed Y on male sterility. The substitution of D. simulans Y chromosome into D. sechellia, and both reciprocal Y chromosome substitutions between D. simulans and D. mauritiana were unsuccessful. Introgressions of cytoplasm between D. simulans and D. mauritiana (or D. sechellia) also did not have any effect on hybrid male sterility. These results rule out the X-Y interaction hypothesis as a general explanation of Haldane's rule in this species group and indicate an involvement of an X-autosome interaction. Models of symmetrical and asymmetrical X-autosome interaction have been developed which explain the Y chromosome substitution results and suggest that evolution of interactions between different genetic elements in the early stages of speciation is more likely to be of an asymmetrical nature. The model of asymmetrical X-autosome interaction also predicts that different sets of interacting genes may be involved in different pairs of related species and can account for the observation that hybrid male sterility in many partially isolated species is often nonreciprocal or unidirectional.