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Spatial population structure: patterns of adaptation in populations of the water hyacinth grasshopper Cornops aquaticum (Bruner 1906)

Published online by Cambridge University Press:  18 August 2021

Pablo C. Colombo
Affiliation:
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Mónica Zelarayán
Affiliation:
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
M. Celeste Franceschini
Affiliation:
CONICET-CECOAL, Corrientes, Argentina
M. Isabel Remis*
Affiliation:
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
*
Author for correspondence: M. Isabel Remis, Email: [email protected]

Abstract

The water hyacinth grasshopper Cornops aquaticum (Bruner 1906) constitutes an appropriate model to assess phenotypic and karyotypic variability in the context of differentiation and adaptation of insect populations because it occurs over a wide latitudinal range. This study represents a general analysis of phenotype, karyotype and molecular variation in native populations of C. aquaticum in South America. This is also relevant because this insect is considered a promising biological control agent of water hyacinth, a native South American aquatic plant but a pest in South Africa. Along Paraná and Uruguay River Basins, body size correlated negatively with latitude, and positively so with temperature and rainfall in both sexes. To test whether the chromosomal and phenotypic patterns were adaptive, we compared them with neutral microsatellite loci variation in populations from the medium and lower course of the Paraná River. Firstly, the lack of pairwise association between karyotype and phenotype distance matrixes with that of neutral loci suggested non-neutrality. Secondly, phenotypic differentiation for all morphometric traits (PST) was significantly larger than molecular differentiation (FST), indicating a prevailing divergence selection effect on the observed phenotypic patterns. Finally, the phenotypic and genotypic spatial structures – inferred from Bayesian approaches – were discordant: neutral genetic structure clustered together most populations except for the two southernmost, downstream ones, whereas phenotypic spatial structure groups together all the deltaic populations and singles out the two northernmost ones. The results suggest directional selection leading to higher centric fusion frequencies in the downstream populations and favouring morphometric optimal differences in relation to the environment.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Adis, J, Bustorf, E, Lhano, MG, Amedegnato, C and Nunes, AL (2007) Distribution of Cornops grasshoppers (Leptysminae: Acrididae: Orthoptera) in Latin America and the Caribbean Islands. Studies on Neotropical Fauna and Environment 42(1), 1124.CrossRefGoogle Scholar
Adis, J, Sperber, C, Brede, EG, Capello, S, Franceschini, MC, Hill, M, Lhano, MG, Marques, M, Nunes, AL and Polar, P (2008) Morphometric differences in the grasshopper Cornops aquaticum (Bruner, 1906) from South America and South Africa. Journal of Orthoptera Research 17(2), 141147.CrossRefGoogle Scholar
Adrion, JR, Hahn, MW and Cooper, BS (2015) Revisiting classic clines in Drosophila melanogaster in the age of genomics. Trends in Genetics 31(8), 434444.CrossRefGoogle ScholarPubMed
Ayala, D, Fontaine, MC, Cohuet, A, Fontenille, D, Vitalis, R and Simard, F (2011) Chromosomal inversions, natural selection and adaptation in the malaria vector Anopheles funestus. Molecular Biology and Evolution 28, 745758.CrossRefGoogle ScholarPubMed
Bai, Y, Dong, JJ, Guan, DL, Xie, JY and Xu, SQ (2016) Geographic variation in wing size and shape of the grasshopper Trilophidia annulata (Orthoptera: Oedipodidae): morphological trait variations follow an ecogeographical rule. Scientific Reports 6, 32680.CrossRefGoogle ScholarPubMed
Berner, D and Blanckenhorn, WU (2006) Grasshopper ontogeny in relation to time constraints: adaptive divergence and stasis. Journal of Animal Ecology 75(1), 130139.CrossRefGoogle ScholarPubMed
Bidau, CJ, Miño, CI, Castillo, ER and Martí, DA (2012) Effects of abiotic factors on the geographic distribution of body size variation and chromosomal polymorphisms in two neotropical grasshopper species (Dichroplus: Melanoplinae: Acrididae). Psyche: A Journal of Entomology 2(863947), 111.Google Scholar
Blackmon, H, Ross, L and Bachtrog, D (2017) Sex determination, sex chromosomes, and karyotype evolution in insects. Journal of Heredity 108, 7893.CrossRefGoogle ScholarPubMed
Blanckenhorn, WU and Demont, M (2004) Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integrative and Comparative Biology 44(6), 413424.CrossRefGoogle ScholarPubMed
Blanckenhorn, WU, Bauerfeind, SS, Berger, D, Davidowitz, G, Fox, CW, Guillaume, F, Nakamura, S, Nishimura, K, Sasaki, H, Stillwell, RC, Tachi, T and Schäfer, MA (2018) Life history traits, but not body size, vary systematically along latitudinal gradients on three continents in the widespread yellow dung fly. Ecography 41, 20802091.CrossRefGoogle Scholar
Blondeau Da Silva, S (2017) Pstat: Assessing P st Statistics. R package version 1.2. Available at https://CRAN.R-project.org/package=Pstat.Google Scholar
Bownes, A, Hill, MP and Byrne, MJ (2010) Evaluating the impact of herbivory by a grasshopper, Cornops aquaticum (Orthoptera: Acrididae), on the competitive performance and biomass accumulation of water hyacinth, Eichhornia crassipes (Pontederiaceae). Biological Control 53(3), 297303.CrossRefGoogle Scholar
Bragg, JG, Supple, MA, Andrew, RL and Borevitz, JO (2015) Genomic variation across landscapes: insights and applications. New Phytology 207, 953967.CrossRefGoogle ScholarPubMed
Brede, EG, Adis, J and Schneider, P (2008) Genetic diversity, population structure and gene flow in native populations of a proposed biocontrol agent (Cornops aquaticum). Biological Journal of the Linnean Society 95(4), 666676.CrossRefGoogle Scholar
Brommer, JE (2011) Whither P st? The approximation of Q st by P st in evolutionary and conservation biology. Journal of Evolutionary Biology 24(6), 11601168.CrossRefGoogle ScholarPubMed
Bruner, L (1906) Synoptic list of Paraguayan Acrididae, or locusts, with descriptions of new forms. Proceedings of the United States National Museum 30(1461), 613694.CrossRefGoogle Scholar
Center, TD, Hill, MP, Cordo, H and Julien, MH (2002). Waterhyacinth. In van Driesche, R, Blossey, B, Hoddle, M, Lyon, S, Reardon, R (eds), Biological Control of Invasive Plants in the Eastern United States. Morgantown: Forest Health and Technology Enterprises Team, pp. 4164.Google Scholar
Chapuis, M, Lecoq, M, Michalakis, Y, Loiseau, A, Sword, GA, Piry, S and Estoup, A (2008) Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles. Molecular Ecology 17(16), 36403653.CrossRefGoogle ScholarPubMed
Charlesworth, D (2015) The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations. Evolutionary Applications 9, 7490.CrossRefGoogle ScholarPubMed
Charlesworth, B and Barton, NH (2018) The spread of an inversion with migration and selection. Genetics 208, 377382.CrossRefGoogle Scholar
Charlesworth, B and Charlesworth, D (1973) Selection of new inversions in multi-locus genetic systems. Genetical Research 21, 167183.CrossRefGoogle Scholar
Coetzee, J, Hill, M, Byrne, M and Bownes, A (2011) A review of the biological control programmes on Eichhornia crassipes (C.Mart.) Solms (Pontederiaceae), Salvinia molesta D.S.Mitch. (Salviniaceae), Pistia stratiotes L. (Araceae), Myriophyllum aquaticum (Vell.) Verdc. (Haloragaceae) and Azolla filiculoides Lam. (Azollaceae) in South Africa. African Entomology 19(2), 451468.CrossRefGoogle Scholar
Colombo, PC (2007) Effects of polymorphic Robertsonian rearrangements on the frequency and distribution of chiasmata in the water-hyacinth grasshopper, Cornops aquaticum (Orthoptera: Acrididae). European Journal of Entomology 104(4), 653659.CrossRefGoogle Scholar
Colombo, PC (2008) Cytogeography of three parallel Robertsonian polymorphisms in the water-hyacinth grasshopper, Cornops aquaticum (Orthoptera: Acrididae). European Journal of Entomology 105(1), 5964.CrossRefGoogle Scholar
Colombo, PC (2009) Metaphase I orientation of Robertsonian trivalents in the water-hyacinth grasshopper, Cornops aquaticum (Acrididae, Orthoptera). Genetics and Molecular Biology 32(1), 9195.CrossRefGoogle Scholar
Colombo, PC (2013) Micro-evolution in grasshoppers mediated by polymorphic robertsonian translocations. Journal of Insect Science 13(43), 122.CrossRefGoogle ScholarPubMed
Colombo, PC and Remis, MI (2018) Phenotypic pattern over centric fusion clinal variation in the water-hyacinth grasshopper, Cornops aquaticum (Orthoptera: Acrididae). European Journal of Entomology 115, 303311.CrossRefGoogle Scholar
Dobzhansky, T (1970) Genetics of the Evolutionary Process. New York, NY: Columbia University Press.Google Scholar
Dumas, D and Britton-Davidian, J (2002) Chromosomal rearrangements and evolution of recombination: comparison of chiasma distribution patterns in standard and Robertsonian populations of the house mouse. Genetics 162(3), 13551366.CrossRefGoogle ScholarPubMed
Endler, JA (1973) Gene flow and population differentiation. Science 179(4070), 243250.CrossRefGoogle ScholarPubMed
Endler, J (1977) Geographic variation, speciation and clines. Monographs in Population Biology 10, 1246.Google ScholarPubMed
Flatt, T (2016) Genomics of clinal variation in Drosophila: disentangling the interactions of selection and demography. Molecular Ecology 25, 10231026.CrossRefGoogle ScholarPubMed
Fouet, C, Gray, E, Besansky, NJ and Costantini, C (2012) Adaptation to aridity in the malaria mosquito Anopheles gambiae: chromosomal inversion polymorphism and body size influence resistance to desiccation. PLoS One 7(4), e34841.CrossRefGoogle ScholarPubMed
Gaskin, JF, Bon, M, Cock, MJ, Cristofaro, M, Biase, AD, Clerck-Floate, RD, Ellison, C, Hinz, H, Hufbauer, R, Julien, M and Sforza, R (2011) Applying molecular-based approaches to classical biological control of weeds. Biological Control 58(1), 121.CrossRefGoogle Scholar
Gopal, B (1987) Aquatic Plant Studies 1: Water Hyacinth. Amsterdam: Elsevier.Google Scholar
Goudet, J and Jombart, T (2015) Package ‘hierfstat’. R package version 0.04-22. Retrieved from http://www.r-project.org, http://github.com/jgx65/hierfstat.Google Scholar
Guerrero, RF and Kirkpatrick, M (2014) Local adaptation and the evolution of chromosome fusions. Evolution 68(10), 27472756.CrossRefGoogle ScholarPubMed
Guillot, G, Renaud, S, Ledevin, R, Michaux, J and Claude, J (2012) A unifying model for the analysis of phenotypic, genetic, and geographic data. Systematic Biology 61(6), 897911.CrossRefGoogle ScholarPubMed
Hausch, S, Shurin, JB and Matthews, B (2013) Variation in body shape across species and populations in a radiation of Diaptomid Copepods. PLoS One 8(6), e68272.CrossRefGoogle Scholar
Hernández, MIM, Monteiro, LR and Favila, ME (2009) The role of body size and shape in understanding competitive interactions within a community of Neotropical dung Beatles. Journal of Insect Science 11, 114.Google Scholar
Hewitt, GM (1979) Orthoptera: grasshoppers and crickets. Animal Cytogenetics 3, 170.Google Scholar
Hoy, MA (2019) Insect population ecology and molecular genetics. In Hoy, MA (ed.), Insect Molecular Genetics : An Introduction to Principles and Applications, 4th Edn. ISBN 9780128152300. Academic Press Boston, pp. 515561.CrossRefGoogle Scholar
Huizenga, K, Shaidle, M, Brinton, J, Gore, L, Ebo, M, Solliday, A, Buguey, P, Whitman, D and Juliano, S (2008) Geographic differences in the body sizes of adult Romalea microptera. Journal of Orthoptera Research 17, 135139.CrossRefGoogle Scholar
Kapun, M and Flatt, T (2018) The adaptive significance of chromosomal inversion polymorphism in Drosophila melanogaster. Molecular Ecology 28(6), 12631282. doi: 10.1111/mec.14871CrossRefGoogle Scholar
Kirk, H and Freeland, JR (2011) Applications and implications of neutral versus non-neutral markers in molecular ecology. International Journal of Molecular Science 12, 39663988.CrossRefGoogle ScholarPubMed
Kirkpatrick, M (2017) The evolution of genome structure by natural and sexual selection. Journal of Heredity 108(1), 311.CrossRefGoogle ScholarPubMed
Kirkpatrick, M and Barton, N (2006) Chromosome inversions, local adaptation and speciation. Genetics 173, 419434.CrossRefGoogle ScholarPubMed
Lehmann, G and Lehmann, A (2008) Variation in body size among populations of the bushcricket Poecilimon thessalicus (Orthoptera: Phaneropteridae): an ecological adaptation. Journal of Orthoptera Research 17, 165169.CrossRefGoogle Scholar
Leinonen, T, O'Hara, R, Cano, JM and Merilä, J (2008) Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. Journal of Evolutionary Biology 21, 117.CrossRefGoogle ScholarPubMed
Leinonen, T, Mccairns, RJ, O'Hara, RB and Merilä, J (2013) Q STF ST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nature Reviews Genetics 14(3), 179190.CrossRefGoogle Scholar
Martin, G, Chapuis, E and Goudet, J (2008) Multivariate Q STF ST comparisons: a neutrality test for the evolution of the G matrix in structured populations. Genetics 180(4), 21352149.CrossRefGoogle Scholar
Matthews, B, Narwani, A, Hausch, S, Nonaka, E, Peter, H, Yamamichi, M, Sullam, KE, Bird, KC, Thomas, MK, Hanley, T.C., TC and Turner, C (2011) Toward an integration of evolutionary biology and ecosystem science. Ecology Letters 14, 690701.CrossRefGoogle ScholarPubMed
Mehta, CR and Patel, NR (1983) A network algorithm for performing fisher's exact test in r × c contingency tables. Journal of the American Statistical Association 78(382), 427.Google Scholar
Messenger, PS and van den Bosch, R (1971) The adaptability of introduced biological control agents. In Huffaker, CB (ed.), Biological Control. Boston, MA: Springer, pp. 6892. doi: 10.1007/978-1-4615-6528-4_3.Google Scholar
Mousseau, TA and Roff, DA (1989) Adaptation to seasonality in a cricket: patterns of phenotypic and genotypic variation in body size and diapause expression along a cline in season length. Evolution 43(7), 14831496.CrossRefGoogle Scholar
Noguerales, V, García-Navas, V, Cordero, PJ and Ortego, J (2016) The role of environment and core-margin effects on range-wide phenotypic variation in a montane grasshopper. Journal of Evolutionary Biology 29(11), 21292142.CrossRefGoogle Scholar
Oberholzer, IG and Hill, MP (2000) How safe is the grasshopper Cornops aquaticum for release on water hyacinth in South Africa? In ACIAR Proceedings (pp. 8288). ACIAR; 1998.Google Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2019) vegan: Community Ecology Package. R package version 2.5-6. Available at https://CRAN.R-project.org/package=vegan.Google Scholar
Ortego, J, Aguirre, MP and Cordero, PJ (2012) Genetic and morphological divergence at different spatiotemporal scales in the grasshopper Mioscirtus wagneri (Orthoptera: Acrididae). Journal of Insect Conservation 16, 103110.CrossRefGoogle Scholar
Pellegrini, MOO, Horn, CN and Almeida, RF (2018) Total evidence phylogeny of Pontederiaceae (Commelinales) sheds light on the necessity of its recircumscription and synopsis of Pontederia L. PhytoKeys 108, 2583.CrossRefGoogle Scholar
Pujol, B, Wilson, AJ, Ross, RI and Pannell, JR (2008) Are Q STF ST comparisons for natural populations meaningful? Molecular Ecology 17(22), 47824785.CrossRefGoogle Scholar
Raeymaekers, JAM, Van Houdt, JKJ, Larmuseau, MHD, Geldof, S and Volckaert, FAM (2007) Divergent selection as revealed by P ST and QTL-based F ST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Molecular Ecology 16, 891905.CrossRefGoogle Scholar
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/. .Google Scholar
Roderick, GK, Hufbauer, R and Navajas, M (2012) Evolution and biological control. Evolutionary Applications 5(5), 419423.CrossRefGoogle ScholarPubMed
Roff, DA and Mousseau, T (2005) The evolution of the phenotypic covariance matrix: evidence for selection and drift in Melanoplus. Journal of Evolutionary Biology 18(4), 11041114.CrossRefGoogle ScholarPubMed
Roman, J and Darling, JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends in Ecology & Evolution 22(9), 454464.CrossRefGoogle ScholarPubMed
Romero, ML, Colombo, PC and Remis, MI (2014) Morphometric differentiation in Cornops aquaticum (Orthoptera: Acrididae): associations with sex, chromosome, and geographic conditions. Journal of Insect Science 14(1), 164. doi: 10.1093/jisesa/ieu026CrossRefGoogle ScholarPubMed
Romero, ML, Colombo, PC and Remis, MI (2017) Microsatellite DNA analysis of population structure in Cornops aquaticum (Orthoptera: Acrididae), over a cline for three Robertsonian translocations. Evolutionary Ecology 31(6), 937953.CrossRefGoogle Scholar
Rosetti, N and Remis, MI (2013) Latitudinal clines in the grasshopper Dichroplus elongatus: coevolution of the A genome and B chromosomes? Journal of Evolutionary Biology 26(4), 719732.CrossRefGoogle ScholarPubMed
Rundle, S, Bilton, D and Foggo, A (2007) By wind, wings or water: body size, dispersal and range size in aquatic invertebrates. In Hildrew, A, Raffaelli, D & Edmonds-Brown, R (eds.), Body Size: The Structure and Function of Aquatic Ecosystems, Ecological Reviews Cambridge: Cambridge University Press, pp. 186209.CrossRefGoogle Scholar
Savolainen, O, Lascoux, M and Merilä, J (2013) Ecological genomics of local adaptation. Nature Reviews Genetics 14, 807820.CrossRefGoogle ScholarPubMed
Schaeffer, SW, Goetting-Minesky, MP, Kovacevic, M, Peoples, JR, Graybill, JL, Miller, JM, Kim, K, Nelson, JG and Anderson, WW (2003) Evolutionary genomics of inversions in Drosophila pseudoobscura: evidence for epistasis. Proceedings of the National Academy of Sciences USA 100, 83198324.CrossRefGoogle ScholarPubMed
Sesarini, C and Remis, MI (2008) Molecular and morphometric variation in chromosomally differentiated populations of the grasshopper Sinipta dalmani (Orthopthera: Acrididae). Genetica 133(3), 295306.CrossRefGoogle Scholar
Seymour, M, Räsänen, K and Kristjánsson, B (2019) Drift versus selection as drivers of phenotypic divergence at small spatial scales: the case of Belgjarskógur threespine stickleback. Ecology and Evolution 9, 81338145. doi: 10.1002/ece3.5381CrossRefGoogle ScholarPubMed
Silva, FR, Marques, MI, Battirola, LD and Lhano, MG (2010) Fenologia de Cornops aquaticum (Bruner) (Orthoptera: Acrididae) em Eichhornia azurea (Pontederiaceae) no norte do Pantanal de Mato Grosso. Neotropical Entomology 39(4), 535542.CrossRefGoogle Scholar
Smith, A and Belk, MC (2018) Does body size affect fitness the same way in males and females? A test of multiple fitness components?. Biological Journal of the Linnean Society 124(1), 4755.CrossRefGoogle Scholar
Spitze, K (1993) Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics 135(2), 367374.CrossRefGoogle ScholarPubMed
Statistica Statsoft Inc. (1996) Statistica 5 for Windows (Computer Program Manual). Tulsa, OK: Statistica.Google Scholar
Stearns, SC (1992) The Evolution of Life Histories. Oxford, United Kingdom: Oxford University Press.Google Scholar
Storz, JF (2002) Contrasting patterns of divergence in quantitative traits and neutral DNA markers: analysis of clinical variation. Molecular Ecology 11, 25372551.CrossRefGoogle Scholar
Taffarel, A, Bidau, CJ and Martí, DA (2015) Chromosome fusion polymorphisms in the grasshopper Dichroplus fuscus (Orthoptera: Acrididae: Melanoplinae): insights on meiotic effects. European Journal of Entomology 112, 1119.CrossRefGoogle Scholar
Taylor, SJ, Downie, D and Paterson, ID (2011) Genetic diversity of introduced populations of the water hyacinth biological control agent Eccritotarsus catarinensis (Hemiptera: Miridae). Biological Control 58, 330336.CrossRefGoogle Scholar
Turić, N, Temunović, M, Radović, A, Vignjević, G, Sudarić Bogojević, M and Merdić, E (2015) Flood pulses drive the temporal dynamics of assemblages of aquatic insects (Heteroptera and Coleoptera) in a temperate floodplain. Freshwater Biology 60(10), 20512065.CrossRefGoogle Scholar
Wajnberg, E (2004) Measuring genetic variation in natural enemies used for biological control. In Ehler, L, Sforza, R and Mateille, T (eds), Why and How? Genetics, Evolution and Biological Control. London, UK: CAB International, pp. 1937.CrossRefGoogle Scholar
Weir, BS and Cockerham, CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6), 1358.Google ScholarPubMed
Wellband, K, Mérot, C, Linnansaari, T, Elliott, J, Curry, R and Bernatchez, L (2018) Chromosomal fusion and life history-associated genomic variation contribute to within-river local adaptation of Atlantic salmon. Molecular Ecology 28, 1439–1459. doi: 10.1111/mec.14965Google ScholarPubMed
Whitlock, MC (2008) Evolutionary inference from Q ST. Molecular Ecology 17, 18851896.CrossRefGoogle ScholarPubMed
Whitman, DW (2008) The significance of body size in the Orthoptera: a review. Journal of Orthoptera Research 12, 117134.CrossRefGoogle Scholar
Wright, S (1951) The genetical structure of populations. Annals of Eugenetics 15, 323354.CrossRefGoogle ScholarPubMed
Wright, S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19(3), 395420.CrossRefGoogle Scholar
Zang, YY, Zhang, DY and Barrett, SCH (2010) Genetic uniformity characterizes the invasive spread of water hyacinth (Eichhornia crassipes), a clonal aquatic plant. Molecular Ecology 19(9), 17741786.CrossRefGoogle Scholar