scholarly journals Genetic incompatibilities do not snowball in a demographic model of speciation

2021 ◽  
Author(s):  
Carlos A. Maya-Lastra ◽  
Deren A. R. Eaton

Two populations evolving in isolation can accumulate genetic differences over time that cause incompatibilities in their hybrid offspring. These “Dobzhansky-Muller incompatibilities” (DMIs) are predicted to accumulate at a rate faster than linear as the number of incompatible gene interactions “snowballs”. Here we show that this snowball prediction is an artifact of two unrealistic modeling assumptions that stem from ignoring demography. We introduce a new alternative “demographic speciation model” in which the rate of DMI accumulation between populations is affected by the efficiency of purifying selection to remove incompatibilities that arise within populations. This model yields new testable predictions for understanding the tempo and mode of speciation based on population demographic parameters. A large-scale empirical analysis of bird and mammal datasets supports a unique prediction of our model: a negative relationship between effective population sizes and speciation rates. Our results challenge views of the snowball theory, and of ecological speciation models rooted in positive selection, showing instead that purifying selection may play a major role in mediating speciation rates.

2019 ◽  
Author(s):  
Andrew Morgan ◽  
Nicholas Brazeau ◽  
Billy Ngasala ◽  
Lwidiko Mhamilawa ◽  
Madeline Denton ◽  
...  

Abstract Background: Tanzania’s Zanzibar archipelago has made significant gains in malaria control over the last decade and is a target for malaria elimination. Despite consistent implementation of effective tools since 2002, elimination has not been achieved. Importation of parasites from outside of the archipelago is thought to be an important cause of malaria’s persistence, but this paradigm has not been studied using modern genetic tools.Methods: We used whole-genome sequencing (WGS) to investigate the impact of importation, employing population genetic analyses of Plasmodium falciparum isolates from both the archipelago and mainland Tanzania. We assessed ancestry, levels of genetic diversity and differentiation, patterns of relatedness, and patterns of selection between these two populations by leveraging recent advances in deconvolution of genomes from polyclonal malaria infections.Results: We identified significant decreases in the effective population sizes in both populations in the timeframe of decreasing malaria transmission in Tanzania. Identity by descent analysis showed that parasites in the two populations shared large sections of their genomes, on the order of 5 cM, suggesting shared ancestry within the last 10 generations. Even with limited sampling,, we demonstrate a pair of isolates between the mainland and Zanzibar that are related at the expected level of half-siblings, consistent with recent importation.Conclusions: These findings suggest that importation plays an increasing role for malaria incidence on Zanzibar and demonstrate the value of genomic approaches for identifying corridors of parasite movement to the island.


2020 ◽  
Author(s):  
Andrew Morgan ◽  
Nicholas Brazeau ◽  
Billy Ngasala ◽  
Lwidiko Mhamilawa ◽  
Madeline Denton ◽  
...  

Abstract Background Tanzania’s Zanzibar archipelago has made significant gains in malaria control over the last decade and is a target for malaria elimination. Despite consistent implementation of effective tools since 2002, elimination has not been achieved. Importation of parasites from outside of the archipelago is thought to be an important cause of malaria’s persistence, but this paradigm has not been studied using modern genetic tools. Methods Whole-genome sequencing (WGS) was used to investigate the impact of importation, employing population genetic analyses of Plasmodium falciparum isolates from both the archipelago and mainland Tanzania. Ancestry, levels of genetic diversity and differentiation, patterns of relatedness, and patterns of selection between these two populations were assessed by leveraging recent advances in deconvolution of genomes from polyclonal malaria infections. Results Significant decreases in the effective population sizes were inferred in both populations that coincide with a period of decreasing malaria transmission in Tanzania. Identity by descent analysis showed that parasites in the two populations shared long segments of their genomes, on the order of 5 cM, suggesting shared ancestry within the last 10 generations. Even with limited sampling, two of isolates between the mainland and Zanzibar were identified that are related at the expected level of half-siblings, consistent with recent importation. Conclusions These findings suggest that importation plays an important role for malaria incidence on Zanzibar and demonstrate the value of genomic approaches for identifying corridors of parasite movement to the island.


2017 ◽  
Vol 9 (11) ◽  
pp. 2987-3007 ◽  
Author(s):  
Pádraic Corcoran ◽  
Toni I Gossmann ◽  
Henry J Barton ◽  
Jon Slate ◽  
Kai Zeng ◽  
...  

Abstract Population genetic theory predicts that selection should be more effective when the effective population size (Ne) is larger, and that the efficacy of selection should correlate positively with recombination rate. Here, we analyzed the genomes of ten great tits and ten zebra finches. Nucleotide diversity at 4-fold degenerate sites indicates that zebra finches have a 2.83-fold larger Ne. We obtained clear evidence that purifying selection is more effective in zebra finches. The proportion of substitutions at 0-fold degenerate sites fixed by positive selection (α) is high in both species (great tit 48%; zebra finch 64%) and is significantly higher in zebra finches. When α was estimated on GC-conservative changes (i.e., between A and T and between G and C), the estimates reduced in both species (great tit 22%; zebra finch 53%). A theoretical model presented herein suggests that failing to control for the effects of GC-biased gene conversion (gBGC) is potentially a contributor to the overestimation of α, and that this effect cannot be alleviated by first fitting a demographic model to neutral variants. We present the first estimates in birds for α in the untranslated regions, and found evidence for substantial adaptive changes. Finally, although purifying selection is stronger in high-recombination regions, we obtained mixed evidence for α increasing with recombination rate, especially after accounting for gBGC. These results highlight that it is important to consider the potential confounding effects of gBGC when quantifying selection and that our understanding of what determines the efficacy of selection is incomplete.


1996 ◽  
Vol 68 (2) ◽  
pp. 151-155 ◽  
Author(s):  
Leslie A. Pray ◽  
Charles J. Goodnight ◽  
Lori Stevens ◽  
James M. Schwartz ◽  
Guiyun Yan

SummaryDespite the increasing number of studies on the magnitude of Ne/N ratios, much remains unknown about the effects of demographic and environmental variables on Ne/N. We determined Ne/N for seven population size treatments, ranging from N = 2 to N = 960, in the red flour beetle Tribolium castaneum. Ne/N decreased with increasing N, as evidenced by a significant negative relationship between log N and Ne/N. Our results are consistent with other published data on the relationship between Ne/N and N. Effective population sizes in large populations may be much smaller than previously recognized. These results have important implications for conservation and evolutionary biology.


2019 ◽  
Author(s):  
Andrew P Morgan ◽  
Nicholas F Brazeau ◽  
Billy Ngasala ◽  
Lwidiko E. Mhamilawa ◽  
Madeline Denton ◽  
...  

ABSTRACTBackgroundTanzania’s Zanzibar archipelago has made significant gains in malaria control over the last decade and is a target for malaria elimination. Despite consistent implementation of effective tools since 2002, elimination has not been achieved. Importation of parasites from outside of the archipelago is thought to be an important cause of malaria’s persistence, but this paradigm has not been studied using modern genetic tools.MethodsWe used whole-genome sequencing (WGS) to investigate the impact of importation, employing population genetic analyses of Plasmodium falciparum isolates from both the archipelago and mainland Tanzania. We assessed ancestry, levels of genetic diversity and differentiation, patterns of relatedness, and patterns of selection between these two populations by leveraging recent advances in deconvolution of genomes from polyclonal malaria infections.ResultsWe identified significant decreases in the effective population sizes in both populations in the timeframe of decreasing malaria transmission in Tanzania. Identity by descent analysis showed that parasites in the two populations shared large sections of their genomes, on the order of 5 cM, suggesting shared ancestry within the last 10 generations. Even with limited sampling,, we demonstrate a pair of isolates between the mainland and Zanzibar that are related at the expected level of half-siblings, consistent with recent importationConclusionsThese findings suggest that importation plays an increasing role for malaria incidence on Zanzibar and demonstrate the value of genomic approaches for identifying corridors of parasite movement to the island.


2020 ◽  
Author(s):  
Andrew Morgan ◽  
Nicholas Brazeau ◽  
Billy Ngasala ◽  
Lwidiko Mhamilawa ◽  
Madeline Denton ◽  
...  

Abstract Background : Tanzania’s Zanzibar archipelago has made significant gains in malaria control over the last decade and is a target for malaria elimination. Despite consistent implementation of effective tools since 2002, elimination has not been achieved. Importation of parasites from outside of the archipelago is thought to be an important cause of malaria’s persistence, but this paradigm has not been studied using modern genetic tools. Methods : We used whole-genome sequencing (WGS) to investigate the impact of importation, employing population genetic analyses of Plasmodium falciparum isolates from both the archipelago and mainland Tanzania. We assessed ancestry, levels of genetic diversity and differentiation, patterns of relatedness, and patterns of selection between these two populations by leveraging recent advances in deconvolution of genomes from polyclonal malaria infections. Results : We identified significant decreases in the effective population sizes in both populations in the timeframe of decreasing malaria transmission in Tanzania. Identity by descent analysis showed that parasites in the two populations shared large sections of their genomes, on the order of 5 cM, suggesting shared ancestry within the last 10 generations. Even with limited sampling, we identified a pair of isolates between the mainland and Zanzibar that are related at the expected level of half-siblings, consistent with recent importation Conclusions : These findings suggest that importation plays an important role for malaria incidence on Zanzibar and demonstrate the value of genomic approaches for identifying corridors of parasite movement to the island.


Genetics ◽  
1999 ◽  
Vol 152 (2) ◽  
pp. 763-773 ◽  
Author(s):  
Peter Beerli ◽  
Joseph Felsenstein

Abstract A new method for the estimation of migration rates and effective population sizes is described. It uses a maximum-likelihood framework based on coalescence theory. The parameters are estimated by Metropolis-Hastings importance sampling. In a two-population model this method estimates four parameters: the effective population size and the immigration rate for each population relative to the mutation rate. Summarizing over loci can be done by assuming either that the mutation rate is the same for all loci or that the mutation rates are gamma distributed among loci but the same for all sites of a locus. The estimates are as good as or better than those from an optimized FST-based measure. The program is available on the World Wide Web at http://evolution.genetics.washington.edu/lamarc.html/.


2016 ◽  
Author(s):  
Sarah J. Lindsay ◽  
Raheleh Rahbari ◽  
Joanna Kaplanis ◽  
Thomas Keane ◽  
Matthew E. Hurles

SummaryRecent whole genome sequencing (WGS) studies have estimated that the human germline mutation rate per basepair per generation (∼1.2−10−8) 1,2 is substantially higher than in mice (3.5-5.4−10−9) 3,4, which has been attributed to more efficient purifying selection due to larger effective population sizes in mice compared to humans.5,6,7. In humans, most germline mutations are paternal in origin and the numbers of mutations per offspring increase markedly with paternal age 2,8,9 and more weakly with maternal age 10. Germline mutations can arise at any stage of the cellular lineage from zygote to gamete, resulting in mutations being represented in different proportion and types of cells, with the earliest embryonic mutations being mosaic in both somatic and germline cells. Here we use WGS of multi-sibling mouse and human pedigrees to show striking differences in germline mutation rate and spectra between the two species, including a dramatic reduction in mutation rate in human spermatogonial stem cell (SSC) divisions, which we hypothesise was driven by selection. The differences we observed between mice and humans result from both biological differences within the same stage of embryogenesis or gametogenesis and species-specific differences in cellular genealogies of the germline.


Genetics ◽  
1999 ◽  
Vol 153 (4) ◽  
pp. 1717-1729 ◽  
Author(s):  
Karl J Schmid ◽  
Loredana Nigro ◽  
Charles F Aquadro ◽  
Diethard Tautz

AbstractWe present a survey of nucleotide polymorphism of three novel, rapidly evolving genes in populations of Drosophila melanogaster and D. simulans. Levels of silent polymorphism are comparable to other loci, but the number of replacement polymorphisms is higher than that in most other genes surveyed in D. melanogaster and D. simulans. Tests of neutrality fail to reject neutral evolution with one exception. This concerns a gene located in a region of high recombination rate in D. simulans and in a region of low recombination rate in D. melanogaster, due to an inversion. In the latter case it shows a very low number of polymorphisms, presumably due to selective sweeps in the region. Patterns of nucleotide polymorphism suggest that most substitutions are neutral or nearly neutral and that weak (positive and purifying) selection plays a significant role in the evolution of these genes. At all three loci, purifying selection of slightly deleterious replacement mutations appears to be more efficient in D. simulans than in D. melanogaster, presumably due to different effective population sizes. Our analysis suggests that current knowledge about genome-wide patterns of nucleotide polymorphism is far from complete with respect to the types and range of nucleotide substitutions and that further analysis of differences between local populations will be required to understand the forces more completely. We note that rapidly diverging and nearly neutrally evolving genes cannot be expected only in the genome of Drosophila, but are likely to occur in large numbers also in other organisms and that their function and evolution are little understood so far.


2019 ◽  
Author(s):  
Eleanor F. Miller ◽  
Rhys E. Green ◽  
Andrew Balmford ◽  
Robert Beyer ◽  
Marius Somveille ◽  
...  

AbstractDuring the Quaternary, large climate oscillations had profound impacts on the distribution, demography and diversity of species globally. Birds offer a special opportunity for studying these impacts because surveys of geographical distributions, publicly-available genetic sequence data, and the existence of species with adaptations to life in structurally different habitats, permit large-scale comparative analyses. We use Bayesian Skyline Plot (BSP) analysis of mitochondrial DNA to reconstruct profiles depicting how effective population size (Ne) may have changed over time, focussing on variation in the effect of the last deglaciation among 102 Holarctic species. Only 3 species showed a decline in Ne since the Last Glacial Maximum (LGM) and 7 showed no sizeable change, whilst 92 profiles revealed an increase in Ne. Using bioclimatic Species Distribution Models (SDMs), we also estimated changes in species potential range extent since the LGM. Whilst most modelled ranges also increased, we found no correlation across species between the magnitude of change in range size and change in Ne. The lack of correlation between SDM and BSP reconstructions could not be reconciled even when range shifts were considered. We suggest the lack of agreement between these measures might be linked to changes in population densities which can be independent of range changes. We caution that interpreting either SDM or BSPs independently is problematic and potentially misleading. Additionally, we found that Ne of wetland species tended to increase later than species from terrestrial habitats, possibly reflecting a delayed increase in the extent of this habitat type after the LGM.


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