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Phenotypic and Genetic Variations in Obligate Parthenogenetic Populations of Eriosoma lanigerum Hausmann (Hemiptera: Aphididae)

  • Ecology, Behavior and Bionomics
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Abstract

The study of phenotypic and genetic variation of obligate parthenogenetic organisms contributes to an understanding of evolution in the absence of genetic variation produced by sexual reproduction. Eriosoma lanigerum Hausmann undergoes obligate parthenogenesis in Mexico City, Mexico, due to the unavailability of the host plants required for sexual reproduction. We analysed the phenotypic and genetic variation of E. lanigerum in relation to the dry and wet season and plant phenology. Aphids were collected on two occasions per season on a secondary host plant, Pyracantha koidzumii, at five different sites in the southern area of Mexico City, Mexico. Thirteen morphological characteristics were measured from 147 to 276 individuals per site and per season. A multivariate analysis of variance was performed to test the effect of the season, site and their interaction on morphological traits. Morphological variation was summarised using a principal component analysis. Genetic variation was described using six enzymatic loci, four of which were polymorphic. Our study showed that the site and season has a significant effect on morphological trait variation. The largest aphids were recorded during cold temperatures with low relative humidity and when the plant was at the end of the fruiting period. The mean genetic diversity was low (mean H e = 0.161), and populations were genetically structured by season and site. Morphological and genetic variations appear to be associated with environmental factors that directly affect aphid development and/or indirectly by host plant phenology.

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References

  • Adams DC, Collyer ML (2009) A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution 63:1143–1154

    Article  PubMed  Google Scholar 

  • Altermatt F (2010) Tell me what you eat and I’ll tell you when you fly: diet can predict phenological changes in response to climate change. Ecol Lett 13:1475–1484

    Article  PubMed  Google Scholar 

  • Anstead JA, Burd JD, Shufran KA (2002) Mitochondrial DNA sequence divergence among Schizaphis graminum (Hemiptera: Aphididae) clones from cultivated and non-cultivated hosts: haplotype and host associations. Bull Entomol Res 92:17–24

    CAS  PubMed  Google Scholar 

  • Arnaud-Haond S, Duarte CM, Alberto F, Serrão EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139

    Article  CAS  PubMed  Google Scholar 

  • Blackman RL (1987) Morphological discrimination of a tobacco-feeding form from Myzus persicae (Sulzer) (Hemiptera: Aphididae), and key to new world Myzus (Nectarosiphon) species. Bull Entomol Res 77:713–730

    Article  Google Scholar 

  • Blackman RL, Eastop VF (2000) Aphids on the world’s crops, an identification and information guide, 2nd edn. Wiley, Chichester, p 251

    Google Scholar 

  • Blackman RL, Spence JM (1994) The effects of temperature on aphid morphology, using a multivariate approach. Eur J Entomol 91:17–22

    Google Scholar 

  • Brown MW, Schmitt JJ, Ranger S, Hogmire HW (1995) Yield reduction in apple by edaphic woolly apple aphid (Homoptera: Aphididae) populations. J Econ Entomol 88:127–133

    Article  Google Scholar 

  • Carletto J, Lombaert E, Chavigny P, Brévault T, Lapchin L, Vanlerberghe-Masutti F (2009) Ecological specialization of the aphid Aphis gossypii Glover on cultivated host plants. Mol Ecol 18:2198–2212

    Article  CAS  PubMed  Google Scholar 

  • Cole RA, Lyn J (1996) Spatial and temporal population structure of Brevicoryne brassicae. Entomol Exp Appl 78:121–127

    Article  Google Scholar 

  • de Barro PJ, Sherratt TN, Carvalho GR, Iyengar A, Maclean N (1995) Geographic and microgeographic genetic differentiation in two aphid species over Southern England using the multilocus (GATA) 4 probe. Mol Ecol 4:375–382

    Article  PubMed  Google Scholar 

  • Delmotte F, Leterme N, Gauthier JP, Rispe C, Simon JC (2002) Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers. Mol Ecol 11:711–723

    Article  CAS  PubMed  Google Scholar 

  • DeLucia EH, Nabity PD, Zavala JA, Berenbaum MR (2012) Climate change: resetting plant-insect interactions. Plant Physiol 160:1677–1685

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dixon AFG (1987) Evolution and adaptive significance of cyclical parthenogenesis in aphids. In: Minks AK, Harrewijn P (eds) World crop pests, aphids their biology, natural enemies and control. Elsevier, Amsterdam, pp 315–320

    Google Scholar 

  • Dixon AFG (1998) Aphid ecology. Chapman & Hall, New York, p 271

    Google Scholar 

  • Eastop VF (1985) The acquisition and processing of taxonomic data. In: Szelegiewicz H (ed) Proceedings. International Aphidological Symposium, Jablona, pp 245–270

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (2009) PHYLIP (Phylogenetic Inference Package) Version 3.69, University of Washington, Seattle, WA. http://evolution.gs.washington.edu/phylip.html

  • Figueroa CC, Loayza-Muro R, Niemeyer HM (2002) Temporal variation of RAPD-PCR phenotype composition of the grain aphid Sitobion avenae (Hemiptera: Aphidade) on wheat: the role of hydroxamic acids. Bull Entomol Res 92:25–33

    CAS  PubMed  Google Scholar 

  • Fisk JH, Carver M, Eastop VF (1992) An electrophoretic study of Eriosoma lanigerum (Hausmann) on apple and Eriosoma sp. from galls on Elm in Canberra, Australia (Hemiptera: Aphididae). Aust J Entomol 31:231–232

    Article  Google Scholar 

  • González de León D (1986) Interespecific hibridization and the cytogenetic architecture of two species of chili papers (Capsicum, Solanaceae). PhD Thesis. University of Reading, UK

  • Guillemaud T, Blin A, Simon S, Morel K, Frank P (2011) Weak spatial and temporal population genetic structure in the Rosy apple aphid Dysaphis plantaginea, in French Apple Orchards. PLoS One 6:e21263. doi:10.1371/journal.pone.0021263

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Haack L, Simon JC, Gauthier JP, Plantegenest M, Dedryver CA (2000) Evidence for predominant clones in a cyclically parthenogenetic organism provided by combined demographic and genetic analyses. Mol Ecol 9:2055–2066

    Article  CAS  PubMed  Google Scholar 

  • Harrison JS, Mondor EB (2011) Evidence for an invasive aphid “superclone”: extremely low genetic diversity in Oleander Aphid (Aphis nerii) populations in the Southern United States. PLoS One 6:e17524. doi:10.1371/journal.pone.0017524

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Heie OE (1987) Morphological structures and adaptations. In: Minks AK, Harrewijn P (eds) World crop pests, aphids their biology, natural enemies and control. Elsevier, Amsterdam, pp 393–400

    Google Scholar 

  • Ibarra V (1988) Delegación Tlalpan. Atlas de la Ciudad de México. Departamento del Distrito Federal, México, p 310

    Google Scholar 

  • SAS Institute (2003) JMP. Statistics and Graphics Guide, version 5.1.01.2. SAS Institute, Cary

    Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Lavandero B, Miranda M, Ramírez CC, Fuentes-Contreras E (2009) Landscape composition modulates population genetic structure of Eriosoma lanigerum (Hausmann) on Malus domestica Borkh in Central Chile. Bull Entomol Res 99:97–105

    Article  CAS  PubMed  Google Scholar 

  • Leal-Aguilar K, Ruiz-Montoya L, Perales H, Morales H (2008) Phenotypic plasticity of Brevicoryne brassicae in responses to nutritional quality of two related host plants. Ecol Entomol 33:735–741

    Google Scholar 

  • Llewellyn KS, Loxdale HD, Harrington R, Brookes CP, Clark SJ, Sunnucks P (2003) Migration and genetic structure of the grain aphid (Sitobion avenae) in Britain related to climate and clonal fluctuation as revealed using microsatellites. Mol Ecol 12:21–34

    Article  CAS  PubMed  Google Scholar 

  • Loxdale HD, Brookes CPI, Wynne R, Clark SJ (1998) Genetic variability within and between English populations of the damson-hop aphid, Phorodun humuli (Hemiptera: Aphididae), with special reference to esterases associated with insecticide resistance. Bull Entomol Res 88:513–526

    Article  Google Scholar 

  • Loxdale HD, Massonnet B, Schöfl G, Weisser WW (2011) Evidence for a quiet revolution: seasonal variation in colonies of the specialist tansy aphid, Macrosiphoniella tanacetaria (Kaltenbach) (Hemitpera: Aphididae) studied using microsatellite markers. Bull Entomol Res 101:221–239

    Article  CAS  PubMed  Google Scholar 

  • Loxdale HD, Vorwerk S, Forneck A (2013) The unestable ‘clone¨: evidence from monitoring AFLP-based mutations for short-term clonal genetic variation in two asexual lineages of the grain aphid, Sitobion avenae (F.). Bull Entomol Res 103:111–118

    Article  CAS  PubMed  Google Scholar 

  • Lushai G, Loxdale HD (2002) The biological improbability of a clone. Genet Res 79:1–9

    Article  PubMed  Google Scholar 

  • Lushai G, Markovithc O, Loxdale HD (2002) Host based genotype variation in insects revisited. Bull Entomol Res 92:159–164

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Gabriel W (1983) Phenotypic evolution and parthenogenesis. Am Nat 122:745–764

    Article  Google Scholar 

  • Manly BFJ (1986) Multivariate statistical methods, a primer, 2nd edn. Chapman and Hall, New York, p 76

    Google Scholar 

  • Massonnet B, Weisser WW (2004) Patterns of genetic differentiation between populations of the specialized herbivore Macrosiphoniella tanacetaria (Homoptera: Aphididae). Heredity 93:1–8

    Article  Google Scholar 

  • Massonnet B, Simon JC, Weisser WW (2002) Metapopulation structure of the specialized herbivore Macrosiphoniella tanacetaria (Homoptera, Aphididae). Mol Ecol 11:2511–2521

    Article  PubMed  Google Scholar 

  • Maudu ME, Mudau FN, Mariga IK (2012) Quality profiles of cultivated and wild bush tea (Athrixia phylicoides) harvested at various phenological stages. Int J Agric Biol 14:552–556

    Google Scholar 

  • Nei M (1977) F-statistics and analysis of genetic diversity in subdivided populations. Ann Hum Genet 41:225–233

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed Central  CAS  PubMed  Google Scholar 

  • Orians CM, Jones CG (2001) Plants as resource mosaics: a functional model for predicting patterns of within-plant resource heterogeneity to consumers based on vascular architecture and local environmental variability. Oikos 94:493–504

    Article  Google Scholar 

  • Parker ED, Niklasson M (2000) Genetic structure and evolution in parthenogenetic animals. In: Singh RS, Krimbas CB (eds) Evolutionary genetics: from molecules to morphology, vol 1. Cambridge University Press, New York, pp 456–474

    Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetics software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnely P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

  • Raboudi F, Makni H, Makni M (2011) Genetic diversity of Potato aphid, Macrosiphum euphorbiae populations in Tunisia detected by RAPD. Afr Entomol 19:133–140

    Article  Google Scholar 

  • Ruiz-Monotya L, Núñez-Farfán J (2013) Testing local adaptation and phnotypic plasticity in a herbivore when alternative related host plants occur sympatrically. PLoS One 8(11):e79070. doi:10.1371/journal.pone.0079070

    Article  Google Scholar 

  • Ruiz-Montoya L, Zúñiga-Bermúdez G, Peña-Martínez R (1994) Morphological variations of Eriosoma lanigerum (Homoptera: Aphididae) on Pyracantha koidzumii in Mexico City. Ann Entomol Soc Am 87:108–115

    Article  Google Scholar 

  • Ruiz-Montoya L, Núñez-Farfán J, Vargas J (2003) Host-associated genetic structure of Mexican populations of the cabbage aphid Brevicoryne brassicae L. (Homoptera: Aphididae). Heredity 91:415–421

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Montoya L, Núñez-Farfán J, Domínguez CA (2005) Changes in morphological traits of the cabbage aphid (Brevicoryne brassicae) induced by the use of different host plants. Ecol Res 20:591–598

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenit trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Shaw CR, Prasad R (1970) Starch gel electrophoresis of enzymes, a compilation of recipes. Biochem Genet 4:297–320

    Article  CAS  PubMed  Google Scholar 

  • Simon JC, Baumann S, Sunnucks P, Hebert PDN, Pierre JS, Le Gallic JF, Dedryver CA (1999) Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers. Mol Ecol 8:531–545

    Article  CAS  PubMed  Google Scholar 

  • Simon JC, Rispe C, Sunnucks P (2002) Ecology and evolution of sex in aphids. Trends Ecol Evol 17:34–39

    Article  Google Scholar 

  • Smith CF (1985) Pemphiginae in North America. In Szelegiewicz H (eds) Evolution and biosystematics of aphids. Proc. International Aphidological Symposium at Jablonna, 5–11 April 1981. Ossolineum, Wroclaw, pp 277–302

  • Sokal RR, Rholf JF (1995) Biometrics, 2nd edn. Freeman, New York

    Google Scholar 

  • Steiner WWM (1987) Electrophoretic techniques for the genetic study of Aphids. In: Minks AK, Harrewijn P (eds) Aphids their biology natural enemies and control, world crop pests 2B. Elsevier, Amsterdam, pp 135–143

    Google Scholar 

  • Sultan SE, Spencer HG (2002) Metapopulation structure favors plasticity over local adaptation. Am Nat 160:271–283

    Article  PubMed  Google Scholar 

  • Sunnucks P, England PR, Taylor AC, Hales D (1996) Microsatellite and chromosome evolution of parthenogenetic Sitiobion aphids in Australia. Genetics 144:747–756

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sunnucks P, de Barro PJ, Lushai G, Maclean N, Hales D (1997) Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Mol Ecol 6:1059–1073

    Article  CAS  PubMed  Google Scholar 

  • Suzuki R, Shimodaira H (2011) pvclust: Hierarchical clustering with P-values vial multiscale Bootstrap resampling. R package version 1.2-2. Http://CRAN.R-project.org/package=pvclust

  • Timm AE, Pringle KL, Warnich L (2005) Genetic diversity of woolly apple aphid Eriosoma lanigerum (Hemiptera: Aphididae) populations in the Western Cae, South Africa. Bull Entomol Res 95:187–191

    Article  CAS  PubMed  Google Scholar 

  • Tomiuk J (1990) Genetic stability in aphid clones and its implication for host plant interactions. In: Campbell RK, Eikenbary RD (eds) Aphid-plant genotype interaction. Elsevier, Amsterdam, pp 275–288

    Google Scholar 

  • Vanlerberghe-Masutti F, Chavigny P (1998) Host-based genetic differentiation in the aphid Aphis gossypii Glover, evidence from RAPD fingerprints. Mol Ecol 7:905–914

    Article  CAS  Google Scholar 

  • Via S (1999) Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53:1446–1457

    Article  Google Scholar 

  • Ward SA (1991) Reproduction and host selection by aphids: the importance of rendezvous hosts. In: Bailey WJ, Ridsdill-Smith J (eds) Reproductive behavior of insects. Chapman and Hall, London, pp 202–226

    Google Scholar 

  • Weber G (1985) Genetic variability in host plant adaptation of the green peach aphid, Myzus persicae. Entomol Exp Appl 38:49–56

    Article  Google Scholar 

  • Wilson ACC, Sunnucks P, Hales DF (1999) Microevolution, low clonal diversity and genetic affinities of parthenogenetic Sitobion aphids in New Zealand. Mol Ecol 8:1655–1666

    Article  PubMed  Google Scholar 

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Acknowledgments

We are grateful for the logistic support provided by Nidia Aldama Gutiérrez. This research was supported by the Secretaría de Investigación y Posgrado del Instituto Politécnico Nacional (SIP-IPN project 1312) and government funding of the Evolutionary Ecology and Conservation line of research at the El Colegio de la Frontera Sur (ECOSUR) Research Centre, Chiapas, Mexico.

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Authors and Affiliations

  1. Depto de Conservación de la Biodiversidad, El Colegio de la Frontera Sur (ECOSUR), Carr. Panamericana y Periférico Sur s/n, C.P. 29290, San Cristóbal de Las Casas, Chiapas, Mexico

    L Ruiz-Montoya

  2. Depto de Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico, Mexico

    G Zúñiga, R Cisneros, Y Salinas-Moreno & R Peña-Martínez

  3. Depto de Conservación de la Biodiversidad, El Colegio de la Frontera Sur (ECOSUR), Chetumal, Quintana Roo, Mexico

    S Machkour-M’Rabet

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  1. L Ruiz-Montoya
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  2. G Zúñiga
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  3. R Cisneros
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Correspondence to L Ruiz-Montoya.

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Ruiz-Montoya, L., Zúñiga, G., Cisneros, R. et al. Phenotypic and Genetic Variations in Obligate Parthenogenetic Populations of Eriosoma lanigerum Hausmann (Hemiptera: Aphididae). Neotrop Entomol 44, 534–545 (2015). https://doi.org/10.1007/s13744-015-0318-1

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