Population genetics of Glossina palpalis palpalis from central African sleeping sickness foci
TL;DR: This first investigation of population genetic structure of G. p.
Abstract: Background: Glossina palpalis palpalis (Diptera: Glossinidae) is widespread in west Africa, and is the main vector of sleeping sickness in Cameroon as well as in the Bas Congo Province of the Democratic Republic of Congo. However, little is known on the structure of its populations. We investigated G. p. palpalis population genetic structure in five sleeping sickness foci (four in Cameroon, one in Democratic Republic of Congo) using eight microsatellite DNA markers. Results: A strong isolation by distance explains most of the population structure observed in our sampling sites of Cameroon and DRC. The populations here are composed of panmictic subpopulations occupying fairly wide zones with a very strong isolation by distance. Effective population sizes are probably between 20 and 300 individuals and if we assume densities between 120 and 2000 individuals per km 2 , dispersal distance between reproducing adults and their parents extends between 60 and 300 meters. Conclusions: This first investigation of population genetic structure of G. p. palpalis in Central Africa has evidenced random mating subpopulations over fairly large areas and is thus at variance with that found in West African populations of G. p. palpalis. This study brings new information on the isolation by distance at a macrogeographic scale which in turn brings useful information on how to organise regional tsetse control. Future investigations should be directed at temporal sampling to have more accurate measures of demographic parameters in order to help vector control decision.
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TL;DR: It is shown that, for organisms collected in a single sample, Wahlund effects and null alleles affect the values of both FIS and FST though in the opposite direction, and a determination key is proposed to interpret data with heterozygote deficits.
Abstract: Null alleles and Wahlund effects are well known causes of heterozygote deficits in empirical population genetics studies as compared to Hardy-Weinberg genotypic expectations. Some authors have theoretically studied the relationship of Wright's FIS computed from subsamples displaying a Wahlund effect and FST before the Wahlund effect, as can occasionally be obtained from populations of long-lived organisms. In the 2 subsample case, a positive relationship between these 2 parameters across loci would represent a signature of Wahlund effects. Nevertheless, for most organisms, getting 2 independent subsamples of the same cohort and population, one with a Wahlund effect and the other without, is almost never achieved and most of the time, empirical population geneticists only collect a single sample, with or without a Wahlund effect, or with or without null alleles. Another issue is that null allele increase FIS and FST altogether and thus may also create such correlation. In this article, I show that, for organisms collected in a single sample, which corresponds to the most common situation, Wahlund effects and null alleles affect the values of both FIS and FST though in the opposite direction. I also show that Wahlund effect produces no or weak positive correlation between the 2 F-statistics, while null alleles generate a strong positive correlation between them. Variation of these F-statistics is small and even minimized for FST under Wahlund effects as compared to null alleles. I finally propose a determination key to interpret data with heterozygote deficits.
71 citations
TL;DR: This simulation study analyzes the behavior of different genetic distances in Island and stepping stone models displaying varying neighborhood sizes and shows that the proportion of null allelic states interact with the slope of the regression of FST/(1−FST) as a function of geographic distance.
Abstract: Studying isolation by distance can provide useful demographic information. To analyze isolation by distance from molecular data, one can use some kind of genetic distance or coalescent simulations. Molecular markers can often display technical caveats, such as PCR-based amplification failures (null alleles, allelic dropouts). These problems can alter population parameter inferences that can be extracted from molecular data. In this simulation study, we analyze the behavior of different genetic distances in Island (null hypothesis) and stepping stone models displaying varying neighborhood sizes. Impact of null alleles of increasing frequency is also studied. In stepping stone models without null alleles, the best statistic to detect isolation by distance in most situations is the chord distance DCSE. Nevertheless, for markers with genetic diversities HS<0.4-0.5, all statistics tend to display the same statistical power. Marginal sub-populations behave as smaller neighborhoods. Metapopulations composed of small sub-population numbers thus display smaller neighborhood sizes. When null alleles are introduced, the power of detection of isolation by distance is significantly reduced and DCSE remains the most powerful genetic distance. We also show that the proportion of null allelic states interact with the slope of the regression of FST/(1-FST) as a function of geographic distance. This can have important consequences on inferences that can be made from such data. Nevertheless, Chapuis and Estoup's FreeNA correction for null alleles provides very good results in most situations. We finally use our conclusions for reanalyzing and reinterpreting some published data sets.
42 citations
TL;DR: Population genetic analyses of Theileria parva from Isoka and Petauke districts showed a low level of genotype exchange between the districts, but a high level of genetic diversity within each district population, implying genetic and geographic sub-structuring between the Districts.
Abstract: Theileriosis, caused by Theileria parva, is an economically important disease in Africa. It is a major constraint to the development of the livestock industry in some parts of eastern, central and southern Africa. In Zambia, theileriosis causes losses of up to 10,000 cattle annually. Cattle blood samples were collected for genetic analysis of Theileria parva from Isoka and Petauke districts in Zambia. Microsatellite analysis was then performed on all Theileria parva positive samples for PCR using a panel of 9 microsatellite markers. Microsatellite data was analyzed using microsatellite toolkit, GenAlEx ver. 6, Fstat ver. 2.9.3.2, and LIAN computer softwares. The combined percentage of positive samples in both districts determined by PCR using the p104 gene primers was 54.9% (95% CI: 46.7 – 63.1%, 78/142), while in each district, it was 44.8% (95% CI: 34.8 – 54.8%) and 76.1% (95% CI = 63.9 – 88.4%) for Isoka and Petauke districts, respectively. We analyzed the population genetic structure of Theileria parva from a total of 61 samples (33 from Isoka and 28 from Petauke) using a panel of 9 microsatellite markers encompassing the 4 chromosomes of Theileria parva. Wright’s F index (FST = 0.178) showed significant differentiation between the Isoka and Petauke populations. Linkage disequilibrium was observed when populations from both districts were treated as a single population. When analyzed separately, linkage disequilibrium was observed in Kanyelele and Kalembe areas in Isoka district, Isoka district overall and in Petauke district. Petauke district had a higher multiplicity of infection than Isoka district. Population genetic analyses of Theileria parva from Isoka and Petauke districts showed a low level of genotype exchange between the districts, but a high level of genetic diversity within each district population, implying genetic and geographic sub-structuring between the districts. The sub-structuring observed, along with the lack of panmixia in the populations, could have been due to low transmission levels at the time of sampling. However, the Isoka population was less diverse than the Petauke population.
36 citations
Cites background from "Population genetics of Glossina pal..."
...Micro- and mini-satellite markers have been used to genotype several species of apicomplexan parasites and their vectors, revealing different population structures [18,21,26-30]....
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TL;DR: This study suggests that different control strategies should be implemented for the three PATTEC blocks and that, given the high potential for re-invasion from island sites, mainland and offshore sites in each block should be targeted at the same time.
Abstract: Glossina fuscipes fuscipes is the primary vector of trypanosomiasis in humans and livestock in Uganda. The Lake Victoria basin has been targeted for tsetse eradication using a rolling carpet initiative, from west to east, with four operational blocks (3 in Uganda and 1 in Kenya), under a Pan-African Tsetse and Trypanosomiasis Eradication Campaign (PATTEC). We screened tsetse flies from the three Ugandan PATTEC blocks for genetic diversity at 15 microsatellite loci from continental and offshore populations to provide empirical data to support this initiative. We collected tsetse samples from 11 sites across the Lake Victoria basin in Uganda. We performed genetic analyses on 409 of the collected tsetse flies and added data collected for 278 individuals in a previous study. The flies were screened across 15 microsatellite loci and the resulting data were used to assess the temporal stability of populations, to analyze patterns of genetic exchange and structuring, to estimate dispersal rates and evaluate the sex bias in dispersal, as well as to estimate demographic parameters (NE and NC). We found that tsetse populations in this region were stable over 4-16 generations and belong to 4 genetic clusters. Two genetic clusters (1 and 2) corresponded approximately to PATTEC blocks 1 and 2, while the other two (3 and 4) fell within PATTEC block 3. Island populations grouped into the same genetic clusters as neighboring mainland sites, suggesting presence of gene flow between these sites. There was no evidence of the stretch of water separating islands from the mainland forming a significant barrier to dispersal. Dispersal rates ranged from 2.5 km per generation in cluster 1 to 14 km per generation in clusters 3 and 4. We found evidence of male-biased dispersal. Few breeders are successfully dispersing over large distances. Effective population size estimates were low (33–310 individuals), while census size estimates ranged from 1200 (cluster 1) to 4100 (clusters 3 and 4). We present here a novel technique that adapts an existing census size estimation method to sampling without replacement, the scheme used in sampling tsetse flies. Our study suggests that different control strategies should be implemented for the three PATTEC blocks and that, given the high potential for re-invasion from island sites, mainland and offshore sites in each block should be targeted at the same time.
28 citations
Cites background or result from "Population genetics of Glossina pal..."
...Solano P, Ravel S, de Meeus T: How can tsetse population genetics contribute to African trypanosomiasis control?...
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...Aylesbury: East Africa European Commission; 2005....
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...Vreysen MJB, Marc JB: Prospects for area-wide integrated control of tsetse flies (Diptera: Glossinidae) and trypanosomosis in sub-Saharan Africa....
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...palpalis palpalis in west and central Africa [17] have provided information that is useful for control efforts at a regional scale....
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...The extent of genetic connectivity of fly populations in this study is congruent with the general finding of other genetic studies on Gff [16,26] and other riverine species of tsetse [13,14,17,80]....
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TL;DR: This study shows that the spatial distribution of traps, as well as the temporal climatic variations might influence entomological and parasitological parameters of HAT and that the presence of perennial water sources in biotopes would favour the development of tsetse flies and thus the transmission of sleeping sickness.
Abstract: Background: Human African Trypanosomiasis (HAT) remains a public health problem in many poor countries. Due to lack of financial resources in these countries, cost-effective strategies are needed for efficient control of this scourge, especially the tsetse vector. It was shown that perennial water sources maintain a favourable biotope for tsetse flies and thus the transmission dynamics of sleeping sickness. The present paper aimed at assessing the transmission dynamics of HAT in a forest environment where the hydrographic network is important. Methods: Two entomological surveys were carried out in July 2009 and March 2010 in the Bipindi sleeping sickness focus of the South Region of Cameroon. Entomological and parasitological data were collected during both trapping periods (including the climate variations throughout a year) and compared to each other. The level of risk for transmission of the disease during each trapping period was also evaluated at the trap level and materialised on the map of the Bipindi focus. Results: Glossina palpalis palpalis was the most prevalent tsetse fly species captured in this focus. The overall densities of tsetse flies as well as the risk for transmission of HAT in the Bipindi focus were significantly higher in July than in March. At the trap level, we observed that these parameters were almost constant, whatever the trapping period, when the biotope included perennial water sources. Conclusions: This study shows that the spatial distribution of traps, as well as the temporal climatic variations might influence entomological and parasitological parameters of HAT and that the presence of perennial water sources in biotopes would favour the development of tsetse flies and thus the transmission of sleeping sickness. These factors should, therefore, be taken into account in order to provide more efficient vector control.
18 citations
Cites result from "Population genetics of Glossina pal..."
...In this study as well as in other studies carried out in the Bipindi sleeping sickness focus [19,22,23], the most prevalent tsetse species was G....
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References
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TL;DR: The World Health Organization (WHO) Expert Committee on HAT Control and Surveillance held in 1995, in consideration of the huge uncertainties between the reported cases and the factual field situation, estimated that the true number of cases was at least 10 times more than reported.
Abstract: One century ago human African trypanosomiasis (HAT), also known as sleeping sickness, was believed to curb the development of colonial territories. As soon as the cause of the disease was clearly identified, colonial authorities established extensive control operations, fearing an unpopulated continent and a shortage of human labour to exploit natural resources. Systematic screening, treatment, and patient follow-up was established in western and central Africa for the gambiense form of the disease while, animal reservoir and vector control was mainly implemented in eastern and southern Africa for the rhodesiense form. By the 1960s, transmission was practically interrupted in all endemic areas, providing evidence that the elimination of the disease as a public health problem was feasible and could be achieved with basic tools. Thereafter, the rarity of cases led to a loss of interest in sustained surveillance, and the risk of re-emergence of the disease was overlooked. Thus in the 1980s the disease re-emerged. By the 1990s, flareups were observed throughout past endemic areas, leading to a worrisome increase in the number of reported cases. At this time, nongovernmental organizations (NGOs) played a crucial role in the control of HAT. However, their interventions were mainly focused on remote and insecure areas. As emergency operators, their policy understandably excluded support to National Sleeping Sickness Control Programmes (NSSCPs), which resulted in (i) the establishment of substitute HAT control systems (ii), the maintenance of a large part of the population at risk out of the umbrella of NGO projects, and (iii) the difficulty for national programmes to sustain control achievements after the NGOs’ withdrawal. Concurrently, bilateral cooperation continued to support NSSCPs in some historically linked countries. Concerning HAT screening, the card agglutination trypanosomiasis test (CATT) for serological screening of populations at risk of HAT gambiense was developed during the 1970s [1], but its large-scale production encountered many problems, hindering its availability [2]; in addition, production of anti-trypanosomal drugs was seriously threatened due to the lower economic return for manufacturers. Research for new diagnostic tools and drugs was scarce [3]. Only eflornithine, initially developed for cancer treatment, was finally registered for the treatment of the gambiense form of the disease in 1990 [4]. But its cost and complex distribution and administration requirements made it inappropriate for the under-equipped peripheral health services in remote rural areas where HAT was prevalent. Only some well-funded NGOs were able to afford the cost of eflornithine treatment. During the 1990s, security constraints due to civil wars and social upheavals complicated HAT control by preventing access to a large number of HAT-endemic areas, leading to difficulties in reaching a large number of affected populations and consequently to a considerable lack of epidemiological information. The World Health Organization (WHO) Expert Committee on HAT Control and Surveillance held in 1995, in consideration of the huge uncertainties between the reported cases and the factual field situation, estimated that the true number of cases was at least 10 times more than reported. Thus from the 30,000 reported cases annually, it was estimated that some 300,000 infected individuals remained ignored in the field [5]. In 1997, the 50th World Health Assembly expressed its concerns about the major recrudescence of cases by adopting a resolution to raise awareness and national and international interest [6]. Subsequently, WHO enhanced its coordinating role and promoted networking with partners, developing a strong advocacy and awareness campaign. As a result, the private sector recognized its responsibility, which led Aventis Pharma and Bayer Health Care to grant in 2001 and 2002 a substantial support to WHO for the control and surveillance of HAT. This support included HAT drug donation and financial contributions that allowed WHO to strengthen its support to diseaseendemic countries (DECs). The importance of the various components of the epidemiology of trypanosomiasis (human, animal, vector control, agricultural activity, and livestock production) and their impact on the development of rural Africa led WHO, in 1995, to promote together with the Food and Agriculture Organization (FAO), the International Atomic Energy Agency (IAEA), and the African Union InterAfrican Bureau for Animal Resources (AUIBAR), an inter-sectoral initiative that ultimately became, in 1997, the Programme Against African Trypanosomiasis (PAAT, http://www.fao.org/ag/againfo/ programmes/en/paat/disease.html). In parallel, African heads of state and governments established during the Afri-
360 citations
"Population genetics of Glossina pal..." refers background in this paper
...After several historical cycles of epidemics followed by decreases in prevalence [1], WHO has recently announced the aim of elimination of HAT as a public health problem [2]....
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TL;DR: Although efforts are still needed to reduce the number of undetected and unreported cases, the comprehensive, village-level mapping of HAT control activities over a ten-year period ensures a detailed and reliable representation of the known geographic distribution of the disease.
Abstract: Background: Following World Health Assembly resolutions 50.36 in 1997 and 56.7 in 2003, the World Health Organization (WHO) committed itself to supporting human African trypanosomiasis (HAT)-endemic countries in their efforts to remove the disease as a public health problem. Mapping the distribution of HAT in time and space has a pivotal role to play if this objective is to be met. For this reason WHO launched the HAT Atlas initiative, jointly implemented with the Food and Agriculture Organization of the United Nations, in the framework of the Programme Against African Trypanosomosis. Results: The distribution of HAT is presented for 23 out of 25 sub-Saharan countries having reported on the status of sleeping sickness in the period 2000 - 2009. For the two remaining countries, i.e. Angola and the Democratic Republic of the Congo, data processing is ongoing. Reports by National Sleeping Sickness Control Programmes (NSSCPs), Non-Governmental Organizations (NGOs) and Research Institutes were collated and the relevant epidemiological data were entered in a database, thus incorporating (i) the results of active screening of over 2.2 million people, and (ii) cases detected in health care facilities engaged in passive surveillance. A total of over 42 000 cases of HAT and 6 000 different localities were included in the database. Various sources of geographic coordinates were used to locate the villages of epidemiological interest. The resulting average mapping accuracy is estimated at 900 m. Conclusions: Full involvement of NSSCPs, NGOs and Research Institutes in building the Atlas of HAT contributes to the efficiency of the mapping process and it assures both the quality of the collated information and the accuracy of the outputs. Although efforts are still needed to reduce the number of undetected and unreported cases, the comprehensive, village-level mapping of HAT control activities over a ten-year period ensures a detailed and reliable representation of the known geographic distribution of the disease. Not only does the Atlas serve research and advocacy, but, more importantly, it provides crucial evidence and a valuable tool for making informed decisions to plan and monitor the control of sleeping sickness.
357 citations
"Population genetics of Glossina pal..." refers background in this paper
...Central Africa, in particular DRC, remains the most affected area by sleeping sickness, harbouring more than 90% of the total number of cases [3]....
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TL;DR: It is demonstrated that a state-biased dispersal can be directly inferred from microsatellite genotype distributions, which opens new perspectives for empirical studies in this area.
Abstract: We investigated dispersal patterns in the monogamous Crocidura russula , based both on direct field observations (mark-recapture data) and on genetic analyses (microsatellite loci). Natal dispersal was found to be low. Most juveniles settled within their natal territory or one immediately adjacent. Migration rate was estimated to two individuals per year and per population. The correlation between genetic and geographical distances over a 16 km transect implies that migration occurs over short ranges. Natal dispersal was restricted to first-litter juveniles weaned in early May; this result suggests a direct dependence of dispersal on reproductive opportunities. Natal dispersal was highly female biased, a pattern unusual among mammals. Its association with monogamy provides support for the resource-competition model of dispersal. Our results demonstrate that a state-biased dispersal can be directly inferred from microsatellite genotype distributions, which opens new perspectives for empirical studies in this area.
353 citations
"Population genetics of Glossina pal..." refers methods in this paper
...First, Weir and Cockerham’s estimate of FST, mean (mAIc) and variance (vAIc) of Favre et al.’s corrected assignment index AIc [36] were computed separately in each sex....
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...We also chose to keep mAIc because it may be more powerful in case of complex patterns of sex specific genetic structures [39,40]....
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...This choice of statistics is motivated by the work of Goudet et al. [37] where vAIc was shown to be the most powerful statistic when migration is low (less than 10%), while FST performs better in other circumstances....
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...Assignment based parameters were in line with a male biased dispersal but only mAIc provided a significant test (P-value = 0.013) (Table 1)....
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...For the sex that has a higher dispersal rate, FST and mAIc are expected to be smaller and vAIc is expected to be higher than for the sex that has a lower dispersal rate (see [38] for more details on these tests)....
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TL;DR: It is suggested here that an indirect estimate of the effective number of breeders might be based on the excess of heterozygosity expected in a cohort of progeny produced by a limited number of males and females.
Abstract: The important parameter of effective population size is rarely estimable directly from demographic data. Indirect estimates of effective population size may be made from genetic data such as temporal variation of allelic frequencies or linkage disequilibrium in cohorts. We suggest here that an indirect estimate of the effective number of breeders might be based on the excess of heterozygosity expected in a cohort of progeny produced by a limited number of males and females. In computer simulations, heterozygote excesses for 30 unlinked loci having various numbers of alleles and allele-frequency profiles were obtained for cohorts produced by samples of breeders drawn form an age-structured population and having known variance in reproductive success and effective number. The 95% confidence limits around the estimate contained the true effective population size in 70 of 72 trials and the Spearman rank correlation of estimated and actual values was 0.991. An estimate based on the heterozygote excess might have certain advantages over the previous estimates, requiring only single-locus and single-cohort data, but the sampling error among individuals and the effect of departures from random union of gametes still need to be explored.
234 citations
"Population genetics of Glossina pal..." refers background in this paper
...[49] (see also [50]) corrected by Balloux [51]....
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TL;DR: The method of estimatingeffective population size from linkage disequilibrium data appears to result in realistic estimates of effective population size when adequate sample size and a sufficient number of polymorphic loci are available.
Abstract: A primary parameter in the assessment of the viability of a population is its effective population size (Ne). Allozyme analysis of four groups of fishes provided data on linkage disequilibrium, which were then used to estimate Ne. The groups included hatchery samples of juvenile white seabass, Atractoscion nobilis, juvenile rainbow trout, Oncorhynchus mykiss, from the Shasta Hatchery, and juvenile chinook salmon, O. tshawytscha, from the Coleman National Fish Hatchery. The fourth sample consisted of juvenile chinook salmon from the threatened winter run in the upper Sacramento River. The groups of fish were chosen to represent different applications of the methodology to conservation of fishes. For a variety of reasons. Ne may be considerably lower than census counts of fish present in the parental populations. The Ne of the hatchery broodstock that produced the sample of juvenile white seabass was estimated to be approximately 10, although 25 adult white seabass were present in a mass spawning tank. Ne estimates for the parental populations of the Shasta and Coleman Hatchery samples were 35.8 and 132.5, respectively. The actual number of fish spawned at the Shasta Hatchery was approximately 40, whereas nearly 10,000 salmon were spawned at the Coleman Hatchery. The threatened winter run of chinook salmon had an estimated Ne of 85.5 and an approximate run size of 2000 salmon. The method of estimating effective population size from linkage disequilibrium data appears to result in realistic estimates of effective population size when adequate sample size and a sufficient number of polymorphic loci are available.
Uno de los parametros fundamentales en la evaluacion de la viabilidad de poblaciones es su tamano poblacional efectivo (Ne). El analisis de alocimas en cuatro grupos de peces proveyo de datos sobre el desequilibrio de ligamiento que luego fueron usados para estimar Ne. Los grupos incluian muestras de Cherna Blanca juvenil, Atractoscion nobilis, y Trucha Arcoiris juvenil, Oncorhynchus mykiss, provenientes del criadero Shasta, y salmon “Chinook” juvenil, O. tshawytscha, provenientes del criadero “Coleman National Fish Hatchery”. La cuarta muestra consistio en juveniles del Salmon “Chinook” provenientes de cardumentes invernales amenazados del curso superior del rijo Sacramento. Los grupos de peces fueron elegidos en forma tal que representasen distintas aplicaciones de la metodologia destinada a la conservacion de peces. Debido a una variedad de razones, Ne puede ser considerablemente menor que el tamano censal de los peces presentes en las poblaciones paternales. El Ne del stock filial de la estacion de cria que produjo la muestra de juveniles de Cerna Blanca fue de aproximadamente 10, si bien el numero de Chernas Blancas adultas presentes en el tanque de desove masivo era 25. Las estimaciones de Ne de las pobalciones paternales de las muestras provenientes de los criaderos Shasta y “Coleman Hatchery,” fueron 35.8 y 132.5, respectivamente. El numero real de peces nacidos en el criadero Shasta fue aproximadamente 40, mientras que cerca de 10.000 salmones fueron procreados en el criadero “Coleman Hatchery”. Los cardumenes invernales del Salmon “Chinook” tuvieron un Ne estimado de 85.5 y un tamano de cardumen de aproximadamente 2.000 salmones. El metodo de estimacion de tamano poblacional efectivo a partir de datos de desequilibrio de ligamiento parece dar como resultado estimaciones nal efectivo cuando se usan tamanos muestrales adecuados y cuando un numero suficiente de loci polimorficos estan disponibles.
177 citations
"Population genetics of Glossina pal..." refers methods in this paper
...The first is Bartley’s method [44], from Hill [45] and modified by Waples [46] and is implemented with NeEstimator [47]....
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