Genetic and morphological variation in sexual and asexual parasitoids of the genus Lysiphlebus – an apparent link between wing shape and reproductive mode

BMC Evolutionary Biology

Christoph Vorburger⁶  Željko Tomanović⁴  Ana Mitrovski Bogdanović⁵  Petr Starý²  Nickolas G Kavallieratos³  Vladimir Žikić¹  Ana Ivanović⁴  Milana Mitrović⁷  Andjeljko Petrović⁴ 

[1] Department of Biology and Ecology, Faculty of Sciences and Mathematics, University of Niš, Višegradska 33, Niš, 18000, Serbia;Laboratory of Aphidology, Institute of Entomology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, České Budějovice, 37005, Czech Republic;Laboratory of Agricultural Zoology and Entomology, Department of Crop Science, Agricultural University of Athens, 75 Iera Odos str., Athens, 11855, Attica, Greece;Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, Belgrade, 11000, Serbia;Institute of Biology and Ecology, Faculty of Science, University of Kragujevac, Radoja Domanovića 12, Kragujevac, 34000, Serbia;Institute of Integrative Biology, ETH Zürich, Switzerland, and EAWAG, Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, Dübendorf, 8600, Switzerland;Department of Plant Pests, Institute for Plant Protection and Environment, Banatska 33, Zemun 11080, Serbia

关键词: COI;    Reproductive mode;    Wing shape;    Parasitoid wasps;   

Others  :  1129199
DOI  :  10.1186/s12862-015-0293-5

 received in 2014-09-01, accepted in 2015-01-22,  发布年份 2015

【 摘 要 】

Background

Morphological divergence often increases with phylogenetic distance, thus making morphology taxonomically informative. However, transitions to asexual reproduction may complicate this relationship because asexual lineages capture and freeze parts of the phenotypic variation of the sexual populations from which they derive. Parasitoid wasps belonging to the genus Lysiphlebus Foerster (Hymenoptera: Braconidae: Aphidiinae) are composed of over 20 species that exploit over a hundred species of aphid hosts, including many important agricultural pests. Within Lysiphlebus, two genetically and morphologically well-defined species groups are recognised: the “fabarum” and the “testaceipes” groups. Yet within each group, sexual as well as asexual lineages occur, and in L. fabarum different morphs of unknown origin and status have been recognised. In this study, we selected a broad sample of specimens from the genus Lysiphlebus to explore the relationship between genetic divergence, reproductive mode and morphological variation in wing size and shape (quantified by geometric morphometrics).

Results

The analyses of mitochondrial and nuclear gene sequences revealed a clear separation between the “testaceipes” and “fabarum” groups of Lysiphlebus, as well as three well-defined phylogenetic lineages within the “fabarum” species group and two lineages within the “testaceipes” group. Divergence in wing shape was concordant with the deep split between the “testaceipes” and “fabarum” species groups, but within groups no clear association between genetic divergence and wing shape variation was observed. On the other hand, we found significant and consistent differences in the shape of the wing between sexual and asexual lineages, even when they were closely related.

Conclusions

Mapping wing shape data onto an independently derived molecular phylogeny of Lysiphlebus revealed an association between genetic and morphological divergence only for the deepest phylogenetic split. In more recently diverged taxa, much of the variation in wing shape was explained by differences between sexual and asexual lineages, suggesting a mechanistic link between wing shape and reproductive mode in these parasitoid wasps.

【 授权许可】

   
2015 Petrovic et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Lande R, Arnold SJ: The measurement of selection on correlated characters. Evolution 1983, 37:1210-26.
• [2]Richardson MK, Chipman AD: Developmental constraints in a comparative framework: a test case using variations in phalanx number during amniote evolution. J Exp Zool B Mol Dev Evol 2003, 296B:8-22.
• [3]Galis F, Metz JAJ: Evolutionary novelties: the making and breaking of pleiotropic constraints. Integr Comp Biol 2007, 47:409-19.
• [4]Blomberg SP, Garland T, Ives AR: Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 2003, 57:717-45.
• [5]Losos JB: Seeing the forest for the trees: the limitations of phylogenies in comparative biology. Am Nat 2011, 177:709-27.
• [6]Losos JB: Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: an evolutionary analysis. Ecol Monograph 1990, 60:369-88.
• [7]Gidaszewski NA, Baylac M, Klingenberg CP: Evolution of sexual dimorphism of wing shape in the Drosophila melanogaster subgroup. BMC Evol Biol 2009, 9:110. BioMed Central Full Text
• [8]Drake AG, Klingenberg CP: Large-scale diversification of skull shape in domestic dogs: disparity and modularity. Am Nat 2010, 175:289-301.
• [9]Sherratt E, Gower DJ, Klingenberg CP, Wilkinson M: Evolution of cranial shape in caecilians (Amphibia: Gymnophiona). Evol Biol 2014, 41:528-45.
• [10]Price PW: Evolutionary biology of parasites. Princeton University Press, Princeton; 1980.
• [11]Strong DR, Lawton JH, Southwood R: Insects on plants. Community patterns and mechanisms. Blackwell Scientific, Oxford; 1984.
• [12]Kavallieratos NG, Tomanović Ž, Starý P, Athanassiou CG, Sarlis GP, Petrović O, et al.: A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of southeastern Europe and their aphid-plant associations. App Entomol Zool 2004, 39:527-63.
• [13]Starý P: Aphid parasitoids of the Czech Republic. Academia, Prague; 2006.
• [14]Starý P, Rakhshani E, Tomanović Ž, Hoelmer K, Kavallieratos NG, Yu J, et al.: A new species of Lysiphlebus Förster 1862 (Hymenoptera: Braconidae: Aphidiinae) attacking soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) from China. J Hymenoptera Res 2010, 19:179-86.
• [15]Petrović A, Mitrović M, Starý P, Petrović-Obradović O, Tomanović Ž, Žikić V, et al.: Lysiphlebus orientalis, a new invasive parasitoid in Europe – evidence from molecular markers. Bull Entomol Res 2013, 103:451-7.
• [16]Ameri M, Rasekh A, Mohammadi Z. A comparison of life history traits of sexual and asexual strains of the parasitoid wasp, Lysiphlebus fabarum (Braconidae: Aphidiinae). Ecol Entomol. 2014. doi:10.1111/een.12155.
• [17]Žikić V, Petrović A, Ivanović A: Allometric shape changes indicate significant divergence in the wing shape between asexual and sexual lineages of Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae). Acta Entomol Serbica. 2014, 19:53-62.
• [18]Cook JM: Sex determination in the Hymenoptera-a review of models and evidence. Heredity 1993, 71:421-35.
• [19]Heimpel GE, de Boer JG: Sex determination in the Hymenoptera. Annu Rev Entomol 2008, 53:209-30.
• [20]Starý P, Tomanović Ž, Petrović O: A new parasitoid of root-feeding aphids from the Balkan mountains (Hymenoptera, Braconidae, Aphidiinae). Deut Entomol Z 1998, 45:175-9.
• [21]Kavallieratos NG, Tomanović Ž: Some rare and endemic aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae) from the Balkan Peninsula. Acta Entomol Serbica. 2001, 6:121-9.
• [22]Belshaw R, Quicke DLJ, Völkl W, Godfray HCJ: Molecular markers indicate rare sex in a predominantly asexual parasitoid wasp. Evolution 1999, 53:1189-99.
• [23]Starý P: Biology and distribution of microbe-associated thelytokous populations of aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae). J Appl Entomol 1999, 123:231-5.
• [24]Sandrock C, Schirrmeister B, Vorburger C: Evolution of reproductive mode variation and host associations in a sexual-asexual complex of aphid parasitoids. BMC Evol Biol 2011, 11:348. doi:10.1186/1471-2148-11-348 BioMed Central Full Text
• [25]Derocles SAP, Le Ralec A, Plantegenest M, Chaubet B, Cruaud C, Cruaud A, et al.: Identification of molecular markers for DNA barcoding in the Aphidiinae (Hym. Braconidae). Mol Ecol Resour 2012, 12:197-208.
• [26]Gilchrist AS, Azevedo RB, Partridge L, O’Higgins P: Adaptation and constraint in the evolution of Drosophila melanogaster wing shape. Evol Dev 2000, 2:114-24.
• [27]Klingenberg CP, Zaklan SD: Morphological integration between developmental compartments in the Drosophila wing. Evolution 2000, 54:1273-85.
• [28]Klingenberg CP, Badyaev AV, Sowry SM, Beckwith NJ: Inferring developmental modularity from morphological integration: analysis of individual variation and asymmetry in bumblebee wings. Amer Nat 2001, 157:11-23.
• [29]Mitrović M, Petrović A, Kavallieratos NG, Starý P, Petrović-Obradović O, Tomanović Ž, et al.: Geographic structure with no evidence for host-associated lineages in European populations of Lysiphlebus testaceipes, an introduced biological control agent. Biol Control 2013, 66:150-8.
• [30]Sandrock C, Vorburger C: Single-locus recessive inheritance of asexual reproduction in a parasitoid wasp. Curr Biol 2011, 21:433-7.
• [31]Engelstädter J, Sandrock C, Vorburger C: Contagious parthenogenesis, automixis, and a sex determination meltdown. Evolution 2011, 65:501-11.
• [32]Carreira VP, Soto IM, Mensch J, Fanara JJ: Genetic basis of wing morphogenesis in Drosophila: sexual dimorphism and non-allometric effects of shape variation. BMC Dev Biol 2011, 11:32. BioMed Central Full Text
• [33]Kavallieratos NG, Lykouressis DP, Sarlis GP, Stathas GJ, Sanchis-Segovia A, Athanassiou CG: The Aphidiinae (Hymenoptera: Ichneumonoidea: Braconidae) of Greece. Phytoparasitica 2001, 29:306-40.
• [34]Sandrock C, Frauenfelder N, von Burg S, Vorburger C: Microsatellite DNA markers for the aphid parasitoid Lysiphlebus fabarum and their applicability to related species. Mol Ecol Notes 2007, 7:1080-3.
• [35]Belshaw R, Quicke DLJ: A molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae). Mol Phylogenet Evol 1997, 7:281-93.
• [36]Campbell BC, Steffen–Campbell JD, Werren JH: Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred froman internal transcribed spacer (ITS2) and 28S rDNA sequences. Insect Mol Biol 1993, 2:225-37.
• [37]Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 1994, 3:294-9.
• [38]Mahuku GS: A simple extraction method suitable for PCR based analysis of plant, fungal, and bacterial DNA. Plant Mol Biol Rep 2004, 22:71-81.
• [39]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-9.
• [40]Zhang DX, Hewitt GM: Nuclear integrations-challenges for mitochondrial- DNA markers. Trends Ecol Evol 1996, 11:247-51.
• [41]Song H, Buhay JE, Whiting MF, Crandall K: Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc Natl Acad Sci U S A 2008, 105:13486-91.
• [42]Kimura M: A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980, 16:111-20.
• [43]Nei M, Kumar S: Molecular evolution and phylogenetics. Oxford University Press, New York; 2000.
• [44]Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-8.
• [45]Tomanović Ž, Kos K, Petrović A, Starý P, Kavallieratos NG, Žikić V, et al.: The relationship between molecular variation and variation in the wing shape of three aphid parasitoid species: Aphidius uzbekistanicus Luzhetzki, Aphidius rhopalosiphi De Stefani Perez and Aphidius avenaphis (Fitch) (Hymenoptera: Braconidae: Aphidiinae). Zool Anz 2013, 252:41-7.
• [46]Rohlf FJ: TpsDig program, version 2.04, ecology and evolution, SUNY at stony brook. State University of New York, New York; 2005.
• [47]Sharkey MJ, Wharton RA: Morphology and terminology. In Manual of the new world genera of the family braconidae (hymenoptera). special publication 1. Edited by Wharton RA, Marsh PM, Sharkey MJ. International Society of Hymenopterists, Washington, DC; 1997:19-37.
• [48]Rohlf FJ, Slice E: Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 1990, 39:40-59.
• [49]Dryden IL, Mardia KV: Statistical shape analysis. Wiley, New York; 1998.
• [50]Klingenberg CP: MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 2011, 11:353-7.
• [51]SAS Institute Inc: Base SAS® 9.1.3: Base SAS® 9.1.3. Procedures Guide. SAS Institute In, Cary, NC; 2009.
• [52]Martins EP, Hansen TF: Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 1997, 149:646-67.
• [53]Rohlf FJ: Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 2001, 55:2143-60.
• [54]Maddison W: Squared-change parsimony reconstructions of ancestral states for continuous-valued characters on a phylogenetic tree. Syst Zool 1991, 40:304-14.
• [55]McArdle B, Rodrigo AG: Estimating the ancestral states of a continuous-valued character using squared-change parsimony: An analytical solution. Syst Biol 1994, 43:573-8.
• [56]Klingenberg CP, Gidaszewski NA: Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Syst Biol 2010, 59:245-61.
• [57]Manly BFJ: Randomization, bootstrap and Monte Carlo methods in biology. Chapman & Hall, London; 1997.