Demographic processes shaping genetic variation of the solitarious phase of the desert locust

Between plagues, the solitarious desert locust (Schistocerca gregaria) is generally thought to exist as small populations, which are particularly prone to extinction events in arid regions of Africa and Asia. Given the high genetic structuring observed in one geographical area (the Eritrean coast) b...

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Published inMolecular ecology Vol. 23; no. 7; pp. 1749 - 1763
Main Authors Chapuis, Marie‐Pierre, Plantamp, Christophe, Blondin, Laurence, Pagès, Christine, Vassal, Jean‐Michel, Lecoq, Michel
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.04.2014
Wiley
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Online AccessGet full text
ISSN0962-1083
1365-294X
1365-294X
DOI10.1111/mec.12687

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Abstract Between plagues, the solitarious desert locust (Schistocerca gregaria) is generally thought to exist as small populations, which are particularly prone to extinction events in arid regions of Africa and Asia. Given the high genetic structuring observed in one geographical area (the Eritrean coast) by former authors, a metapopulation dynamics model involving repeated extinction and colonization events was favoured. In this study, we assessed the validity of a demographic scenario involving temporary populations of the solitarious phase of the desert locust by analysing large‐scale population genetic data. We scored 24 microsatellites in 23 solitarious population samples collected over most of the species range during remission. We found very little genetic structuring and little evidence of declining genetic diversity. A Bayesian clustering method distinguished four genetically differentiated units. Three groups were largely consistent with three population samples which had undergone recent bottleneck events. Nevertheless, the last genetically homogeneous unit included all individuals from the remaining 18 population samples and did not show evidence of demographic disequilibrium. An approximate Bayesian computation treatment indicated a large population size for this main genetic group, moderately reduced between plague and remission but still containing tens of thousands of individuals. Our results diverge from the hypothesis of a classical metapopulation dynamics model. They instead support the scenario in which large populations persist in the solitarious phase of the desert locust.
AbstractList Between plagues, the solitarious desert locust (Schistocerca gregaria) is generally thought to exist as small populations, which are particularly prone to extinction events in arid regions of Africa and Asia. Given the high genetic structuring observed in one geographical area (the Eritrean coast) by former authors, a metapopulation dynamics model involving repeated extinction and colonization events was favoured. In this study, we assessed the validity of a demographic scenario involving temporary populations of the solitarious phase of the desert locust by analysing large-scale population genetic data. We scored 24 microsatellites in 23 solitarious population samples collected over most of the species range during remission. We found very little genetic structuring and little evidence of declining genetic diversity. A Bayesian clustering method distinguished four genetically differentiated units. Three groups were largely consistent with three population samples which had undergone recent bottleneck events. Nevertheless, the last genetically homogeneous unit included all individuals from the remaining 18 population samples and did not show evidence of demographic disequilibrium. An approximate Bayesian computation treatment indicated a large population size for this main genetic group, moderately reduced between plague and remission but still containing tens of thousands of individuals. Our results diverge from the hypothesis of a classical metapopulation dynamics model. They instead support the scenario in which large populations persist in the solitarious phase of the desert locust. [PUBLICATION ABSTRACT]
Between plagues, the solitarious desert locust ( Schistocerca gregaria ) is generally thought to exist as small populations, which are particularly prone to extinction events in arid regions of Africa and Asia. Given the high genetic structuring observed in one geographical area (the Eritrean coast) by former authors, a metapopulation dynamics model involving repeated extinction and colonization events was favoured. In this study, we assessed the validity of a demographic scenario involving temporary populations of the solitarious phase of the desert locust by analysing large‐scale population genetic data. We scored 24 microsatellites in 23 solitarious population samples collected over most of the species range during remission. We found very little genetic structuring and little evidence of declining genetic diversity. A Bayesian clustering method distinguished four genetically differentiated units. Three groups were largely consistent with three population samples which had undergone recent bottleneck events. Nevertheless, the last genetically homogeneous unit included all individuals from the remaining 18 population samples and did not show evidence of demographic disequilibrium. An approximate Bayesian computation treatment indicated a large population size for this main genetic group, moderately reduced between plague and remission but still containing tens of thousands of individuals. Our results diverge from the hypothesis of a classical metapopulation dynamics model. They instead support the scenario in which large populations persist in the solitarious phase of the desert locust.
Between plagues, the solitarious desert locust (Schistocerca gregaria) is generally thought to exist as small populations, which are particularly prone to extinction events in arid regions of Africa and Asia. Given the high genetic structuring observed in one geographical area (the Eritrean coast) by former authors, a metapopulation dynamics model involving repeated extinction and colonization events was favoured. In this study, we assessed the validity of a demographic scenario involving temporary populations of the solitarious phase of the desert locust by analysing large-scale population genetic data. We scored 24 microsatellites in 23 solitarious population samples collected over most of the species range during remission. We found very little genetic structuring and little evidence of declining genetic diversity. A Bayesian clustering method distinguished four genetically differentiated units. Three groups were largely consistent with three population samples which had undergone recent bottleneck events. Nevertheless, the last genetically homogeneous unit included all individuals from the remaining 18 population samples and did not show evidence of demographic disequilibrium. An approximate Bayesian computation treatment indicated a large population size for this main genetic group, moderately reduced between plague and remission but still containing tens of thousands of individuals. Our results diverge from the hypothesis of a classical metapopulation dynamics model. They instead support the scenario in which large populations persist in the solitarious phase of the desert locust.Between plagues, the solitarious desert locust (Schistocerca gregaria) is generally thought to exist as small populations, which are particularly prone to extinction events in arid regions of Africa and Asia. Given the high genetic structuring observed in one geographical area (the Eritrean coast) by former authors, a metapopulation dynamics model involving repeated extinction and colonization events was favoured. In this study, we assessed the validity of a demographic scenario involving temporary populations of the solitarious phase of the desert locust by analysing large-scale population genetic data. We scored 24 microsatellites in 23 solitarious population samples collected over most of the species range during remission. We found very little genetic structuring and little evidence of declining genetic diversity. A Bayesian clustering method distinguished four genetically differentiated units. Three groups were largely consistent with three population samples which had undergone recent bottleneck events. Nevertheless, the last genetically homogeneous unit included all individuals from the remaining 18 population samples and did not show evidence of demographic disequilibrium. An approximate Bayesian computation treatment indicated a large population size for this main genetic group, moderately reduced between plague and remission but still containing tens of thousands of individuals. Our results diverge from the hypothesis of a classical metapopulation dynamics model. They instead support the scenario in which large populations persist in the solitarious phase of the desert locust.
Between plagues, the solitarious desert locust (Schistocerca gregaria) is generally thought to exist as small populations, which are particularly prone to extinction events in arid regions of Africa and Asia. Given the high genetic structuring observed in one geographical area (the Eritrean coast) by former authors, a metapopulation dynamics model involving repeated extinction and colonization events was favoured. In this study, we assessed the validity of a demographic scenario involving temporary populations of the solitarious phase of the desert locust by analysing large-scale population genetic data. We scored 24 microsatellites in 23 solitarious population samples collected over most of the species range during remission. We found very little genetic structuring and little evidence of declining genetic diversity. A Bayesian clustering method distinguished four genetically differentiated units. Three groups were largely consistent with three population samples which had undergone recent bottleneck events. Nevertheless, the last genetically homogeneous unit included all individuals from the remaining 18 population samples and did not show evidence of demographic disequilibrium. An approximate Bayesian computation treatment indicated a large population size for this main genetic group, moderately reduced between plague and remission but still containing tens of thousands of individuals. Our results diverge from the hypothesis of a classical metapopulation dynamics model. They instead support the scenario in which large populations persist in the solitarious phase of the desert locust.
Author Pagès, Christine
Lecoq, Michel
Plantamp, Christophe
Vassal, Jean‐Michel
Blondin, Laurence
Chapuis, Marie‐Pierre
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Keywords microsatellite
pest
Bayesian inference
Orthoptera
population dynamics
bottleneck
Language English
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Fig. S1 Posterior probability densities for the mutation-scaled effective population sizes during plague (A, B) and remission (C, D) periods, when considering log-uniform distributions of the effective population size priors. Fig. S2 Allele frequency distributions for the 24 microsatellites. Fig. S3 Inbreeding coefficient distributions. Fig. S4 Hierarchical Structure clustering analyses based on the Coulon et al.'s () approach.Table S1 Prior distributions for diyabc demographic and mutational parameters. Table S2 Bias and precision of effective population size estimation using diyabc. Table S3 Mean, median and 2.5 and 97.5% quantile estimates from diyabc posterior distribution samples of demographic parameters, when considering log-uniform distributions of the effective population size priors. Table S4 Genetic diversity for 23 S. gregaria population samples at all 24 microsatellite markers. Table S5 Pairwise FST values (Weir ) for 23 S. gregaria population samples (above the diagonal) and confidence intervals based on 2000 bootstrap samples (below diagonal) for all 24 microsatellite markers. Table S6 Pairwise FST values (Weir ) 23 S. gregaria population samples for the 21 microsatellite markers at selective neutrality (above the diagonal) and confidence intervals based on 2000 bootstrap samples (below diagonal). Table S7 Robustness of diyabc inferences on the intensity of the population size decline associated with the end of plagues (α) to rejection and estimation procedures.
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Waloff Z (1966) The upsurges and recessions of the desert locust plague: an historical survey. Anti-Locust Memoir, 8, 111 p.
Wright S (1951) The genetical structure of populations. Annuals of Eugenics, 15, 323-354.
Zhivotovsky LA, Feldman MW, Grishechkin SA (1997) Biased mutations and microsatellite variation. Molecular Biology and Evolution, 14, 926-933.
Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.
Rainey RC (1963) Meteorology and the migration of Desert Locusts. Applications of synoptic meteorology in locust control. Anti-Locust Memoirs, 7, 125 p.
Estoup A, Beaumont M, Sennedot F et al. (2004) Genetic analysis of complex demographic scenarios: spatially expanding populations of the cane toad. Bufo marinus. Evolution, 58, 2021-2036.
Magor JL, Lecoq M, Hunter DM (2008) Preventive control and desert locust plagues. Crop Protection, 27, 1527-1533.
Rosenberg J, Burt PJA (1999) Windborne displacements of Desert Locusts from Africa to the Caribbean and South America. Aerobiologia, 15, 161-175.
Blondin L, Badisco L, Pagès C et al. (2013) Characterization and comparison of microsatellite markers derived from genomic and expressed libraries for the desert locust. Journal of Applied Entomology, 137, 673-683.
Hamilton G, Stoneking M, Excoffier L (2005) Molecular analysis reveals tighter social regulation of immigration in patrilocal populations than in matrilocal populations. Proceedings of the National Academy of Sciences USA, 102, 7476-7480.
Sword GA, Lecoq M, Simpson SJ (2010) Phase polyphenism and preventative locust management. Journal of Insect Physiology, 56, 949-957.
Farrow RA (1975) The African Migratory Locust in its main outbreak area of the middle Niger: quantitative studies of solitary populations in relation to environmental factors. Locusta, 11, 1-198.
Lecoq M, Andriamaroahina TRZ, Solofonaina H et al. (2011) Ecology and population dynamics of solitary Red locusts in Southern Madagascar. Journal of Orthoptera Research, 20, 141-158.
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution, 43, 258-275.
Yassin YA, Heist EJ, Ibrahim KM (2006) PCR primers for polymorphic microsatellite loci in the Desert locust, Schistocerca gregaria (Orthoptera: Acrididae). Molecular Ecology Notes, 6, 784-786.
Pope LC, Estoup A, Moritz C (2000) Phylogeography and population structure of an ecotonal marsupial, Bettongia tropica, determined using mtDNA and microsatellites. Molecular Ecology, 9, 2041-2053.
Garza JC, Williamson E (2001) Detection of reduction in population size using data from microsatellite DNA. Molecular Ecology, 10, 305-318.
Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity, 90, 502-503.
Loader CR (1996) Local likelihood density estimation. Annals of Statistics, 24, 1602-1618.
Weir BS (1996) Genetic Data Analysis II. Sinauer Associates, Sunderland, Massachusetts.
Latchininsky AV, Launois-Luong MH (1997) Le Criquet pèlerin (Schistocerca gregaria Forskål, 1775) dans la partie nord orientale de son aire d'invasion. Les Acridiens, vol. 29. CIRAD, Montpellier/VIZR Saint Petersbourg, 192 p.
Motro U, Thomson G (1982) On heterozygosity and the effective size of populations subject to size changes. Evolution, 36, 1059-1066.
Zhang J, Nei M (1996) Evolution of antennapedia-class homeobox genes. Genetics, 142, 295-303.
R Development Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Cissé S, Ghaout S, Mazih A et al. (2013) Effect of vegetation on density thresholds of adult desert locust gregarization from survey data in Mauritania. Entomologia Experimentalis et Applicata, 149, 159-165.
Girod C, Vitalis R, Leblois R et al. (2011) Inferring population decline and expansion from microsatellite data: a simulation-based evaluation of the MSVAR method. Genetics, 188, 165-179.
Whitlock MC, Barton NH (1997) The effective size of a subdivided population. Genetics, 146, 427-441.
Ellis PE, Carlisle DB, Osborne DJ (1965) Desert locusts: sexual maturation delayed by feeding on senescent vegetation. Science, 149, 546-547.
Menu F, Roebuck JP, Viala M (2000) Bet-hedging diapauses strategies in stochastic environments. American Naturalist, 155, 724-734.
Storey JD, Tibshirani R (2003) Statistical significance for genome-wide studies. Proceedings of the National Academy of Sciences, USA, 100, 9440-9445.
Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics, 5, 299-314.
Chapuis M-P, Popple J-A, Berthier K et al. (2011) Challenges to assessing connectivity between massive populations of the Australian Plague locust. Proceedings of the Royal Society of London, Series B, 278, 3152-3160.
Cornuet J-M, Pudlo P, Veyssier J et al. (2014) DIYABC v2.0: a software to make Approximate Bayesian Computation inferences about population history using Single Nucleotide Polymorphism, DNA sequence and microsatellite data. Bioinformatics, doi: 10.1093/bioinformatics/btt763.
Duranton JF, Lecoq M (1990) Le criquet pèlerin au sahel, Collection Acridologie Opérationnelle, no. 6. CILSS/DFPV, Niamey, Niger.
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Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9, 1322-1332.
Coulon A, Fitzpatrick JW, Bowman R et al. (2008) Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub-jay (Aphelocoma coerulescens). Molecular Ecology, 17, 1685-1701.
Rao YR (1942) Some results of the studies on the desert locust (Schistocerca gregaria Forsk.) in India. Bulletin of Entomological Research, 33, 241-265.
Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genetical Research, 22, 201-204.
Popov GB (1997) Atlas of Desert Locust Breeding Habitats. Food and Agriculture Organization, Rome.
Beaumont MA, Zhang WY, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics, 162, 2025-2035.
Uvarov BP (1966) Grasshoppers and Locusts, vol. 1. Cambridge University Press, Cambridge, UK.
Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity, 103, 285-298.
Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620.
Vesey-Fitzgerald DF (1957) The vegetation of central and eastern Arabia. Journal of Ecology, 45, 779-798.
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program with label switching and multimodality in analysis of population structure. Bioinformatics, 3, 1801-1806.
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Ge
2010; 56
2010; 10
2011; 278
1965; 149
1989; 43
1964; 49
1963; 40
2000; 9
2002; 11
1976
2004; 4
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2008; 8
1996; 144
1996; 263
1975; 11
1996; 142
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1997; 146
1990
2005; 102
1997; 14
2008; 27
1999; 15
2002; 88
2011; 20
1987
2007; 3
1996; 5
1996; 24
1999; 90
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2012; 21
2009; 18
2001; 10
1957; 45
1982; 36
2012
2000; 67
1995; 57
2013; 149
1966; 8
2008; 17
1997
1996
2006; 6
1996; 92
2000; 155
2011; 4
2003; 30
1973; 22
2002; 162
1963; 7
2004; 58
2013; 137
1994; 120
2009; 9
2014
1951; 15
1977; 12
1957; 28
2001; 159
2009; 103
2003; 100
2011; 188
2003; 21
2005; 14
1942; 33
1966
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  publication-title: Journal of Orthoptera Research
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  year: 2008
  end-page: 1533
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  publication-title: Molecular Ecology Resources
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  end-page: 1618
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  publication-title: Genetical Research
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  publication-title: Molecular Ecology
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Snippet Between plagues, the solitarious desert locust (Schistocerca gregaria) is generally thought to exist as small populations, which are particularly prone to...
Between plagues, the solitarious desert locust ( Schistocerca gregaria ) is generally thought to exist as small populations, which are particularly prone to...
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SourceType Open Access Repository
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StartPage 1749
SubjectTerms Africa
Animal behavior
Animal populations
Animals
Arid zones
Asia
Bayes Theorem
Bayesian inference
bottleneck
Cluster Analysis
Evolution
extinction
Genetic diversity
Genetic Variation
genetics
Genetics, Population
Grasshoppers
Grasshoppers - genetics
Insects
Life Sciences
Linkage Disequilibrium
Mass extinctions
Metapopulations
microsatellite
Microsatellite Repeats
Models, Biological
Orthoptera
pest
plague
Population Density
Population Dynamics
Population genetics
Population number
population size
remission
Schistocerca gregaria
Species extinction
Title Demographic processes shaping genetic variation of the solitarious phase of the desert locust
URI https://api.istex.fr/ark:/67375/WNG-HFC2MQDX-M/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fmec.12687
https://www.ncbi.nlm.nih.gov/pubmed/24502250
https://www.proquest.com/docview/1509904932
https://www.proquest.com/docview/1510709911
https://www.proquest.com/docview/1516745403
https://www.proquest.com/docview/1999951789
https://hal.science/hal-02072967
Volume 23
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