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PLOS ONE  2011 

The First Molecular Phylogeny of Strepsiptera (Insecta) Reveals an Early Burst of Molecular Evolution Correlated with the Transition to Endoparasitism

DOI: 10.1371/journal.pone.0021206

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Abstract:

A comprehensive model of evolution requires an understanding of the relationship between selection at the molecular and phenotypic level. We investigate this in Strepsiptera, an order of endoparasitic insects whose evolutionary biology is poorly studied. We present the first molecular phylogeny of Strepsiptera, and use this as a framework to investigate the association between parasitism and molecular evolution. We find evidence of a significant burst in the rate of molecular evolution in the early history of Strepsiptera. The evolution of morphological traits linked to parasitism is significantly correlated with the pattern in molecular rate. The correlated burst in genotypic-phenotypic evolution precedes the main phase of strepsipteran diversification, which is characterised by the return to a low and even molecular rate, and a period of relative morphological stability. These findings suggest that the transition to endoparasitism led to relaxation of selective constraint in the strepsipteran genome. Our results indicate that a parasitic lifestyle can affect the rate of molecular evolution, although other causal life-history traits correlated with parasitism may also play an important role.

References

[1]  O'Conner TD, Mundy NI (2009) Genotype-phenotype associations: substitution models to detect evolutionary associations between phenotypic variables and genotypic evolutionary rate. Bioinformatics 25: i94–i100.
[2]  Lanfear R, Welch JJ, Bromham L (2010) Watching the clock: studying variation in rates of molecular evolution between species. Trends Ecol Evol 25: 495–503.
[3]  Kathirithamby J (1989) Review of the order Strepsiptera. Syst Entomol 14: 41–62.
[4]  Kathirithamby J (2009) Host-parasitoid associations in Strepsiptera. Annu Rev Entomol 54: 227–249.
[5]  Kathirithamby J, Ross LD, Johnston JS (2003) Masquerading as self? endoparasitic Strepsiptera (Insecta) enclose themselves in host-derived epithelial bag. P Natl Acad Sci USA 100: 7655–7659.
[6]  Gillespie JJ, McKenna CH, Yoder MJ, Gutell RR, Johnston JS, et al. (2005) Assessing the odd secondary structural properties of nuclear small subunit ribosomal RNA sequences (18S) of the twisted-wing parasites (Insecta: Strepsiptera). Insect Mol Biol 14: 625–643.
[7]  Pohl H, Beutel RG (2007) The evolution of Strepsiptera. Zoology 111: 318–338.
[8]  McMahon DP, Hayward A, Kathirithamby J (2009) The mitochondrial genome of the ‘twisted-wing parasite’ Mengenilla australiensis: a comparative study. BMC Genomics 10: 603.
[9]  Hunter MS, Woolley JB (2001) Evolution and behavioural ecology of heteronomous aphelinid parasitoids. Annu Rev Entomol 46: 251–90.
[10]  Hayward A, McMahon DP, Kathirithamby J (2011) Cryptic diversity and host specificity in a parasitoid where the sexes utilize hosts from separate orders. Mol Ecol 20: 1508–1528.
[11]  Eggleton P, Belshaw R (1992) Insect parasitoids: an evolutionary overview. Philos Trans R Soc London Ser B 337: 1–20.
[12]  Kinzelbach RK (1978) Strepsiptera. Die Tierwelt Deutschlands 65: 166.
[13]  Poulin R, Morand S (2004) Parasite biodiversity. Washington DC: Smithsonian Institution Press.
[14]  Poulin R, Keeney DB (2008) Host specificity under molecular and experimental scrutiny. Trends Parasitol 24: 24–28.
[15]  Dorus S, Evans PD, Wyckoff GJ, Choi SS, Lahn BT (2004) Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat Genet 36: 1326–1329.
[16]  Nadeau NJ, Burke T, Mundy NI (2007) Evolution of an avian pigmentation gene correlates with a measure of sexual selection. Proc R Soc B Biol Sci 255: 37–45.
[17]  Ramm SA, Oliver PL, Ponting CP, Stockley P, Emes RD (2008) Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Mol Biol Evol 25: 207–219.
[18]  Ahrens D, Ribera I (2009) Inferring speciation modes in a clade of Iberian chafers from rates of morphological evolution in different character systems. BMC Evol Biol 9: 234.
[19]  Kim H, Lee W, Lee S (2010) Morphometric relationship, phylogenetic correlation, and character evolution in the species-rich genus Aphis (Hemiptera: Aphididae). PLoS ONE 5: e11608.
[20]  Hardman M, Hardman LM (2008) The relative importance of body size and paleoclimatic change as explanatory variables influencing lineage diversification rate: an evolutionary analysis of bullhead catfishes (Siluriformes: Ictaluridae). Syst Biol 57: 116–130.
[21]  Omland KE (1997) Correlated rates of molecular and morphological evolution. Evolution 51: 1381–1393.
[22]  Bromham L, Woolfit M, Lee MSY, Rambaut A (2002) Testing the relationship between morphological and molecular rates of change along phylogenies. Evolution 56: 1921–1930.
[23]  Ekman S, Andersen HL, Wedin M (2007) The limitations of ancestral state reconstruction and the evolution of the Ascus in the Lecanorales (lichenized Ascomycota). Syst Biol 57: 141–156.
[24]  Whiting MF, Carpenter JC, Wheeler QD, Wheeler WC (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst Biol 46: 1–68.
[25]  Huelsenbeck JP (1998) Systematic bias in phylogenetic analysis: is the Strepsiptera problem solved? Syst Biol 47: 519–537.
[26]  Huelsenbeck JP (2001) A Bayesian perspective of the Strepsiptera problem. Tidjschr Ent 144: 165–178.
[27]  Wiegmann BM, Trautwein MD, Kim JW, Cassel BK, Bertone MA, et al. (2009) Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biology 7: 34.
[28]  Longhorn SJ, Pohl H, Vogler AP (2010) Ribosomal protein genes of holometabolous insects reject the Halteria, instead revealing a close affinity of Strepsiptera with Coloeptera. Mol Phylogenet Evol 55: 846–859.
[29]  Mckenna DD, Farrell BD (2010) 9-genes reinforce the phylogeny of Holometabola and yield alternative views on the phylogenetic placement of Strepsiptera. PLoS ONE 5: e11887.
[30]  Ishiwata K, Saski G, Owaga J, Miyata T, Su ZH (2010) Phylogenetic relationships among insect orders based on three nuclear protein-coding gene sequences. Mol Phylogenet Evol. (doi:10.1016/j.ympev.2010.11.001).
[31]  Bromham L (2009) Why do species vary in their rate of molecular evolution? Biol Lett 5: 401–404.
[32]  Dowton M, Austin AD (1995) Increased genetic diversity in mitochondrial genes is correlated with the evolution of parasitism in the Hymenoptera. J Mol Evol 41: 958–965.
[33]  Duff RJ, Nickrent DL (1997) Characterization of mitochondrial small-subunit ribosomal RNAs from holoparasitic plants. J Mol Evol 45: 631–639.
[34]  Pohl H, Beutel RG (2005) The phylogeny of Strepsiptera (Hexapoda). Cladistics 21: 328–374.
[35]  Brower AVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. P Natl Acad Sci USA 91: 6491–6495.
[36]  Farrell BD (2001) Evolutionary assembly of the milkweed fauna: cytochrome oxidase I and the age of Tetraopes beetles. Mol Phylogenet Evol 18: 46–478.
[37]  Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, et al. (2007) The delayed rise of present-day mammals. Nature 446: 507–512.
[38]  Ricklefs RE, Losos JB, Townsend TM (2007) Evolutionary diversification of clades of squamate reptiles. J Evol Biol 20: 1751–1762.
[39]  Silvestri F (1943) Studi sugli ‘Strepsiptera’ Insecta. III. Descrizione e biologia di 6 specie italiane di Mengenilla. Boll Lab Zool Gen Agric Portici 32: 197–282.
[40]  Pohl H, Beutel RG (2004) Fine structure of adhesive devices of Strepsiptera (Insecta). Arthropod Struct Dev 33: 31–43.
[41]  Moore BR, Donoghue MJ (2007) Correlates of diversification in the plant clade Dipsacales: geographic movement and evolutionary innovation. Am Nat 170: S28–S55.
[42]  Venditti C, Meade A, Pagel M (2009) Phylogenies reveal new interpretation of speciation and the red queen. Nature 463: 349–352.
[43]  Welch JJ, Bininda-Emonds ORP, Bromham L (2008) Correlates of substitution rate variation in mammalian protein-coding sequences. BMC Evol Biol 8: 53.
[44]  Schmid-Hempel P (2008) Parasite immune evasion: a momentous molecular war. Trends Ecol Evol 23: 318–26.
[45]  Welch JJ, Bromham L (2005) Molecular dating when rates vary. Trends Ecol Evol 20: 320–327.
[46]  Ho SYW (2009) An examination of phylogenetic models of substitution rate variation among lineages. Biol Lett 5: 421–424.
[47]  Crowson RA (1960) The phylogeny of Coleoptera. Ann Rev Entomol 5: 111–134.
[48]  Lartillot N, Philippe H (2004) A Bayesian mixture model for across-site heterogeneities in the amino acid replacement process. Mol Biol Evol 21: 1095–109.
[49]  Bravo F, Pohl H, Silvo-Neto A, Beutel RG (2009) Bahiaxenidae, a “living fossil” and a new family of Strepsiptera (Hexapoda) discovered in Brazil. Cladistics 25: 1–10.
[50]  Castro LR, Dowton M (2005) The position of the Hymenoptera within the Holometabola as inferred from the mitochondrial genome of Perga condei (Hymenoptera: Symphyta: Pergidae). Mol Phylogenet Evol 34: 469–479.
[51]  Castro LR, Dowton M (2006) Mitochondrial genomes in the Hymenoptera and their utility as phylogenetic markers. Syst Entomol 32: 60–69.
[52]  Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95–98.
[53]  Kjer KM, Baldridge GD, Fallon AM (1994) Mosquito large subunit ribosomal RNA: simultaneous alignment of primary and secondary structure. Biochim Biophys Acta 1217: 147–155.
[54]  Gillespie JJ (2004) Characterizing regions of ambiguous alignment caused by the expansion and contraction of hairpin-stem loops in ribosomal RNA molecules. Mol Phylogenet Evol 33: 936–943.
[55]  Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406–3415.
[56]  Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.
[57]  Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564–577.
[58]  Huelsenbeck J, Ronquist F (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17: 754–755.
[59]  Ronquist F, Huelsenbeck JP (2003) MrBayes 3, Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
[60]  Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
[61]  Drummond A, Strimmer K (2001) PAL: An object-oriented programming library for molecular evolution and phylogenetics. Bioinformatics 17: 662–663.
[62]  Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.
[63]  Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105.
[64]  Stomatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
[65]  Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Heredity 92: 371–373.
[66]  Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26: 1–7.
[67]  Strimmer K, von Haeseler A (1997) Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci USA 94: 6815–6819.
[68]  Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502–504.
[69]  Adachi J, Hasegawa M (1996) Model of amino acid substitution in proteins encoded by mitochondrial DNA. J Mol Evol 42: 459–468.
[70]  Abascal F, Posada D, Zardoya R (2007) MtArt: A new model of amino acid replacement for Arthropoda. Mol Biol Evol 24: 1–5.
[71]  Le SQ, Gascuel O (2008) LG: an improved, general amino-acid replacement matrix. Mol Biol Evol 25: 1307–20.
[72]  Rambaut A, Drummond AJ (2007) Tracer v1.4, Available from http://beast.bio.ed.ac.uk/Tracer.
[73]  Stomatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
[74]  Rambaut A, Drummond AJ (2007) FigTree v1.0, Available from http://tree.bio.ed.ac.uk/FigTree.
[75]  Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
[76]  Yang Z (2007) PAML 4, a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591.
[77]  Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4: e88.
[78]  Shapiro B, Rambaut A, Drummond AJ (2006) Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23: 7–9.
[79]  Robinson-Rechavi M, Huchon D (2000) RRTree: Relative-rate tests between groups of sequences on a phylogenetic tree. Bioinformatics 16: 296–297.
[80]  Nee S, Barraclough TG, Harvey PH (1996) Temporal changes in biodiversity: detecting patterns and identifying causes. In: Gaston KJ, editor. Biodiversity: a biology of numbers and differences. Oxford: Blackwell Science. pp. 230–252.
[81]  Rambaut A, Harvey PH, Nee S (1997) End-Epi: an application for inferring phylogenies and population dynamic processes from molecular sequences. Comput Appl Biosci 13: 303–306.
[82]  Rabosky DL (2006) Likelihood methods for inferring temporal shifts in diversification rates. Evolution 60: 1152–1164.
[83]  Chan KM, Moore BR (2005) SYMMETREE: whole-tree analysis of differential diversification rates. Bioinformatics 21: 1709–1710.
[84]  Pagel M, Meade A, Barker D (2004) Bayesian estimation of ancestral character states on phylogenies. Syst Biol 53: 673–684.
[85]  Kathirithamby J, Hayward A, McMahon DP, Ferreira RS, Andreazze R, et al. (2010) Conspecifics of a heterotrophic heteronomous species of Strepsiptera (Insecta) are matched by molecular characterization. Syst Entomol 35: 234–242.
[86]  Pohl H, Kinzelbach KJ (2001) First record of a female stylopid (Strepsiptera: ?Myrecolacidae) parasite of prionomyrmecine ant (Hymenoptera: Formicidae) in Baltic amber. Insect Syst Evol 32: 143–146.
[87]  Maddison WP, Maddison DR (2006) Mesquite, a modular system for evolutionary analysis, Version 1.12. Available at: http://mesquiteproject.org.
[88]  Felsenstein J (1989) PHYLIP-phylogeny inference package (version 3.2). Cladistics 5: 164–166.
[89]  Soria-Carrasco V, Talavera G, Idea J, Castresana J (2007) The K tree score: quantification of differences in the relative branch length and topology of phylogenetic trees. Bioinformatics 23: 2954–2956.

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