Particle and Fibre Toxicology | |
Cuticular differences associated with aridity acclimation in African malaria vectors carrying alternative arrangements of inversion 2La | |
Zainulabeuddin Syed3  Nora J Besansky3  Cheng Liu2  Fang Liu1  Changde Cheng3  Kyanne R Reidenbach3  | |
[1] Department of Applied and Computational Mathematics and Statistics, University of Notre Dame, Notre Dame, IN 46556, USA;Center for Research Computing, University of Notre Dame, Notre Dame, IN 46556, USA;Eck Institute for Global Health & Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA | |
关键词: M and S molecular forms; GC-MS; Desiccation resistance; Cuticle; Chromosomal inversion; Cuticular hydrocarbons; An. coluzzii; An. gambiae; | |
Others : 807312 DOI : 10.1186/1756-3305-7-176 |
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received in 2014-03-06, accepted in 2014-03-31, 发布年份 2014 | |
【 摘 要 】
Background
Principal malaria vectors in Africa, An. gambiae and An. coluzzii, share an inversion polymorphism on the left arm of chromosome 2 (2La/2L+a) that is distributed non-randomly in the environment. Genomic sequencing studies support the role of strong natural selection in maintaining steep clines in 2La inversion frequency along environmental gradients of aridity, and physiological studies have directly implicated 2La in heat and desiccation tolerance, but the precise genetic basis and the underlying behavioral and physiological mechanisms remain unknown. As the insect cuticle is the primary barrier to water loss, differences in cuticle thickness and/or epicuticular waterproofing associated with alternative 2La arrangements might help explain differences in desiccation resistance.
Methods
To test that hypothesis, two subcolonies of both An. gambiae and An. coluzzii were established that were fixed for alternative 2La arrangements (2La or 2L+a) on an otherwise homosequential and shared genetic background. Adult mosquitoes reared under controlled environmental conditions (benign or arid) for eight days post-eclosion were collected and analyzed. Measurements of cuticle thickness were made based on scanning electron microscopy, and cuticular hydrocarbon (CHC) composition was evaluated by gas chromatography–mass spectrometry.
Results
After removing the allometric effects of body weight, differences in mean cuticle thickness were found between alternative 2La karyotypes, but not between alternative environments. Moreover, the thicker cuticle of the An. coluzzii 2La karyotype was contrary to the known higher rate of water loss of this karyotype relative to 2L+a. On the other hand, quantitative differences in individual CHCs and overall CHC profiles between alternative karyotypes and environmental conditions were consistent with expectation based on previous physiological studies.
Conclusions
Our results suggest that alternative arrangements of the 2La inversion are associated with differences in cuticle thickness and CHC composition, but that only CHC composition appears to be relevant for desiccation resistance. Differences in the CHC composition were consistent with previous findings of a lower rate of water loss for the 2L+a karyotype at eight days post-eclosion, suggesting that CHC composition is an important strategy for maintaining water balance in this genetic background, but not for 2La. Despite a higher rate of water loss at eight days, higher body water content of the 2La karyotype confers a level of desiccation resistance equivalent to that of the 2L+a karyotype.
【 授权许可】
2014 Reidenbach et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Sturtevant AH: A Case of Rearrangement of Genes in Drosophila. Proc Natl Acad Sci U S A 1921, 7:235-237.
- [2]Kirkpatrick M, Barton N: Chromosome inversions, local adaptation and speciation. Genetics 2006, 173:419-434.
- [3]Hoffmann AA, Rieseberg LH: Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Ann Rev Ecol Evol Syst 2008, 39:21-42.
- [4]Schaeffer SW: Selection in heterogeneous environments maintains the gene arrangement polymorphism of Drosophila pseudoobscura. Evolution 2008, 62:3082-3099.
- [5]Dobzhansky T: Genetics of the Evolutionary Process. New York: Columbia University Press; 1970.
- [6]Powell JR: Progress and Prospects in Evolutionary Biology: The Drosophila Model. Oxford: Oxford University Press; 1997.
- [7]Krimbas CB, Powell JR: Drosophila inversion polymorphism. London: CRC Press; 1992.
- [8]Rodriguez-Trelles F: Seasonal cycles of allozyme-by-chromosomal-inversion gametic disequilibrium in Drosophila subobscura. Evolution 2003, 57:839-848.
- [9]Etges WJ, Arbuckle KL, Levitan M: Long-term frequency shifts in the chromosomal polymorphisms of Drosophila robusta in the Great Smoky Mountains. Biol J Linn Soc 2006, 88:131-141.
- [10]Balanya J, Oller JM, Huey RB, Gilchrist GW, Serra L: Global genetic change tracks global climate warming in Drosophila subobscura. Science 2006, 313:1773-1775.
- [11]Singh RS, Hickey DA, David J: Genetic differentiation between geographically distant populations of Drosophila melanogaster. Genetics 1982, 101:235-256.
- [12]Hoffmann AA, Weeks AR: Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 2007, 129:133-147.
- [13]Ayala D, Caro-Riano H, Dujardin JP, Rahola N, Simard F, Fontenille D: Chromosomal and environmental determinants of morphometric variation in natural populations of the malaria vector Anopheles funestus in Cameroon. Infect Genet Evol 2011, 11:940-947.
- [14]Rocca KA, Gray EM, Costantini C, Besansky NJ: 2La chromosomal inversion enhances thermal tolerance of Anopheles gambiae larvae. Malar J 2009, 8:147. BioMed Central Full Text
- [15]Fouet C, Gray E, Besansky NJ, Costantini C: Adaptation to aridity in the malaria mosquito Anopheles gambiae: chromosomal inversion polymorphism and body size influence resistance to desiccation. PLoS ONE 2012, 7:e34841.
- [16]Brooke BD, Hunt RH, Chandre F, Carnevale P, Coetzee M: Stable chromosomal inversion polymorphisms and insecticide resistance in the malaria vector mosquito Anopheles gambiae (Diptera: Culicidae). J Med Entomol 2002, 39:568-573.
- [17]Gray EM, Rocca KA, Costantini C, Besansky NJ: Inversion 2La is associated with enhanced desiccation resistance in Anopheles gambiae. Malar J 2009, 8:215. BioMed Central Full Text
- [18]Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibaly MB, Besansky NJ: Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 2013, 3619:246-274.
- [19]World Health Organisation: World Malaria Report: 2013. http://www.who.int/malaria/publications/world_malaria_report_2013/en/ webcite
- [20]Della Torre A, Tu Z, Petrarca V: On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. Insect Biochem Mol Biol 2005, 35:755-769.
- [21]Pombi M, Caputo B, Simard F, Di Deco MA, Coluzzi M, Della Torre A, Costantini C, Besansky NJ, Petrarca V: Chromosomal plasticity and evolutionary potential in the malaria vector Anopheles gambiae sensu stricto: insights from three decades of rare paracentric inversions. BMC Evol Biol 2008, 8:309. BioMed Central Full Text
- [22]White BJ, Cheng C, Sangare D, Lobo NF, Collins FH, Besansky NJ: The population genomics of trans-specific inversion polymorphisms in Anopheles gambiae. Genetics 2009, 183:275-288.
- [23]Cheng C, White BJ, Kamdem C, Mockaitis K, Costantini C, Hahn MW, Besansky NJ: Ecological genomics of Anopheles gambiae along a latitudinal cline: a population-resequencing approach. Genetics 2012, 190:1417-1432.
- [24]Coluzzi M, Sabatini A, Petrarca V, Di Deco MA: Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans R Soc Trop Med Hyg 1979, 73:483-497.
- [25]Petrarca V, Sabatinelli G, Di Deco MA, Papakay M: The Anopheles gambiae complex in the Federal Islamic Republic of Comoros (Indian Ocean): some cytogenetic and biometric data. Parassitologia 1990, 32:371-380.
- [26]Rishikesh N, Di Deco MA, Petrarca V, Coluzzi M: Seasonal variations in indoor resting Anopheles gambiae and Anopheles arabiensis in Kaduna, Nigeria. Acta Trop 1985, 42:165-170.
- [27]Coluzzi M, Sabatini A, Petrarca V, Di Deco MA: Behavioural divergences between mosquitoes with different inversion karyotypes in polymorphic populations of the Anopheles gambiae complex. Nature 1977, 266:832-833.
- [28]White BJ, Hahn MW, Pombi M, Cassone BJ, Lobo NF, Simard F, Besansky NJ: Localization of candidate regions maintaining a common polymorphic inversion (2La) in Anopheles gambiae. PLoS Genet 2007, 3:e217.
- [29]Marron MT, Markow TA, Kain KJ, Gibbs AG: Effects of starvation and desiccation on energy metabolism in desert and mesic Drosophila. J Insect Physiol 2003, 49:261-270.
- [30]Gibbs AG, Chippindale AK, Rose MR: Physiological mechanisms of evolved desiccation resistance in Drosophila melanogaster. J Exp Biol 1997, 200:1821-1832.
- [31]Parkash R, Ranga P: Sex-specific divergence for adaptations to dehydration stress in Drosophila kikkawai. J Exp Biol 2013, 216:3301-3313.
- [32]Benoit JB: Water management by dormant insects: comparisons between dehydration resistance during summer aestivation and winter diapause. Prog Mol Subcell Biol 2010, 49:209-229.
- [33]Chown SL, Sorensen JG, Terblanche JS: Water loss in insects: an environmental change perspective. J Insect Physiol 2011, 57:1070-1084.
- [34]Hadley NF: Water relations of terrestrial arthropods. San Diego: Academic Press; 1994.
- [35]Benoit JB, Denlinger DL: Meeting the challenges of on-host and off-host water balance in blood-feeding arthropods. J Insect Physiol 2010, 56:1366-1376.
- [36]Gibbs AG, Rajpurohit S: Cuticular lipids and water balance. In Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology. Edited by Blomquist GJ, Bagnères A-G. Cambridge: Cambridge University Press; 2010:100-120.
- [37]Wood O, Hanrahan S, Coetzee M, Koekemoer L, Brooke B: Cuticle thickening associated with pyrethroid resistance in the major malaria vector Anopheles funestus. Parasit Vectors 2010, 3:67. BioMed Central Full Text
- [38]Awolola TS, Oduola OA, Strode C, Koekemoer LL, Brooke B, Ranson H: Evidence of multiple pyrethroid resistance mechanisms in the malaria vector Anopheles gambiae sensu stricto from Nigeria. Trans R Soc Trop Med Hyg 2009, 103:1139-1145.
- [39]Vontas J, David JP, Nikou D, Hemingway J, Christophides GK, Louis C, Ranson H: Transcriptional analysis of insecticide resistance in Anopheles stephensi using cross-species microarray hybridization. Insect Mol Biol 2007, 16:315-324.
- [40]Vannini L, Reed TW, Willis JH: Temporal and spatial expression of cuticular proteins of Anopheles gambiae implicated in insecticide resistance or differentiation of M/S incipient species. Parasit Vectors 2014, 7:24. BioMed Central Full Text
- [41]Zhang J, Goyer C, Pelletier Y: Environmental stresses induce the expression of putative glycine-rich insect cuticular protein genes in adult Leptinotarsa decemlineata (Say). Insect Mol Biol 2008, 17:209-216.
- [42]Lee CE, Frost BW: Morphological stasis in the Eurytemora affinis species complex (Copepoda: Temoridae). Hydrobiologia 2002, 480:111-128.
- [43]White BJ, Santolamazza F, Kamau L, Pombi M, Grushko O, Mouline K, Brengues C, Guelbeogo W, Coulibaly M, Kayondo JK, Sharakhov I, Simard F, Petrarca V, Della Torre A, Besansky NJ: Molecular karyotyping of the 2La inversion in Anopheles gambiae. Am J Trop Med Hyg 2007, 76:334-339.
- [44]Lobo NF, Sangare DM, Regier AA, Reidenbach KR, Bretz DA, Sharakhova MV, Emrich SJ, Traore SF, Costantini C, Besansky NJ, Collins FH: Breakpoint structure of the Anopheles gambiae 2Rb chromosomal inversion. Malar J 2010, 9:293. BioMed Central Full Text
- [45]Della Torre A: Polytene chromosome preparation from anopheline mosquitoes. In Molecular Biology of Disease Vectors: A Methods Manual. Edited by Crampton & Hall JM, Beard CB, Louis C. London: Chapman; 1997:329-336.
- [46]Lleonart J, Salat J, Torres GJ: Removing allometric effects of body size in morphological analysis. J Theor Biol 2000, 205:85-93.
- [47]Tabachnick B, Fidell L: Using multivariate statistics. New York: Harper Collins; 1989.
- [48]Sutherst R, Maywald G, Skarratt D: Predicting insect distributions in a changed climate. In Insects in a changing environment. Edited by Harrington R, Stork N. London: Academic Press; 1995:59-91.
- [49]Bayoh MN, Thomas CJ, Lindsay SW: Mapping distributions of chromosomal forms of Anopheles gambiae in West Africa using climate data. Med Vet Entomol 2001, 15:267-274.
- [50]Lindsay SW, Parson L, Thomas CJ: Mapping the ranges and relative abundance of the two principal African malaria vectors, Anopheles gambiae sensu stricto and An. arabiensis, using climate data. Proc R Soc Lond B Biol Sci 1998, 265:847-854.
- [51]Costantini C, Ayala D, Guelbeogo WM, Pombi M, Some CY, Bassole IHN, Ose K, Fotsing J-M, Sagnon NF, Fontenille D, Besansky NJ, Simard F: Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecol 2009, 9:16. BioMed Central Full Text
- [52]Simard F, Ayala D, Kamdem GC, Etouna J, Ose K, Fotsing J-M, Fontenille D, Besansky NJ, Costantini C: Ecological niche partitioning between the M and S molecular forms of Anopheles gambiae in Cameroon: the ecological side of speciation. BMC Ecol 2009, 9:17. BioMed Central Full Text
- [53]Lee Y, Meneses CR, Fofana A, Lanzaro GC: Desiccation resistance among subpopulations of Anopheles gambiae s.s. from Selinkenyi, Mali. J Med Entomol 2009, 46:316-320.
- [54]Cassone BJ, Mouline K, Hahn MW, White BJ, Pombi M, Simard F, Costantini C, Besansky NJ: Differential gene expression in incipient species of Anopheles gambiae. Mol Ecol 2008, 17:2491-2504.
- [55]Papandreou NC, Iconomidou VA, Willis JH, Hamodrakas SJ: A possible structural model of members of the CPF family of cuticular proteins implicating binding to components other than chitin. J Insect Physiol 2010, 56:1420-1426.
- [56]Caputo B, Dani FR, Horne GL, N'Fale S, Diabate A, Turillazzi S, Coluzzi M, Costantini C, Priestman AA, Petrarca V, della Torre A: Comparative analysis of epicuticular lipid profiles of sympatric and allopatric field populations ofAnopheles gambiae s.s. molecular forms andAn. arabiensisfrom Burkina Faso (West Africa). Insect Biochem Mol Biol 2007, 37:389-398.
- [57]Caputo B, Dani FR, Horne GL, Petrarca V, Turillazzi S, Coluzzi M, Priestman AA, Della Torre A: Identification and composition of cuticular hydrocarbons of the major Afrotropical malaria vector Anopheles gambiae s.s. (Diptera: Culicidae): analysis of sexual dimorphism and age-related changes. J Mass Spectrom 2005, 40:1595-1604.
- [58]Benoit JB, Denlinger DL: Suppression of water loss during adult diapause in the northern house mosquito, Culex pipiens. J Exp Biol 2007, 210:217-226.
- [59]Benoit JB, Lopez-Martinez G, Phillips ZP, Patrick KR, Denlinger DL: Heat shock proteins contribute to mosquito dehydration tolerance. J Insect Physiol 2010, 56:151-156.
- [60]Benoit JB, Lopez-Martinez G, Teets NM, Phillips SA, Denlinger DL: Responses of the bed bug, Cimex lectularius, to temperature extremes and dehydration: levels of tolerance, rapid cold hardening and expression of heat shock proteins. Med Vet Entomol 2009, 23:418-425.
- [61]Lehmann T, Dao A, Yaro AS, Adamou A, Kassogue Y, Diallo M, Sekou T, Coscaron-Arias C: Aestivation of the African malaria mosquito, Anopheles gambiae in the Sahel. Amer J Trop Med Hyg 2010, 83:601-606.
- [62]Adamou A, Dao A, Timbine S, Kassogue Y, Yaro AS, Diallo M, Traore SF, Huestis DL, Lehmann T: The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel. Malar J 2011, 10:151. BioMed Central Full Text
- [63]Powell JR, Petrarca V, Della Torre A, Caccone A, Coluzzi M: Population structure, speciation, and introgression in the Anopheles gambiae complex. Parassitologia 1999, 41:101-113.