Genomic and chemical evidence for local adaptation in resistance to different herbivores in Datura stramonium.
Datura stramonium
identity by descent
local adaptation
phenotypic selection
plant-herbivore interactions
resistance
Journal
Evolution; international journal of organic evolution
ISSN: 1558-5646
Titre abrégé: Evolution
Pays: United States
ID NLM: 0373224
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
received:
12
05
2020
revised:
28
08
2020
accepted:
12
09
2020
pubmed:
17
9
2020
medline:
1
6
2021
entrez:
16
9
2020
Statut:
ppublish
Résumé
Because most species are collections of genetically variable populations distributed to habitats differing in their abiotic/biotic environmental factors and community composition, the pattern and strength of natural selection imposed by species on each other's traits are also expected to be highly spatially variable. Here, we used genomic and quantitative genetic approaches to understand how spatially variable selection operates on the genetic basis of plant defenses to herbivores. To this end, an F
Substances chimiques
Alkaloids
0
Banques de données
Dryad
['10.5061/dryad.bnzs7h489']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2629-2643Subventions
Organisme : Consejo Nacional de Ciencia y Tecnología
ID : 2016-2/1527
Organisme : Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT), UNAM
ID : PAPIIT-DGAPA AG200717
Informations de copyright
© 2020 The Authors. Evolution © 2020 The Society for the Study of Evolution.
Références
Agrawal, A. A. 2005. Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evol. Ecol. Res. 7:651-667.
Agrawal, A. A., A. P. Hastings, M. T. J. Johnson, J. L. Maron, and J. P. Salminen. 2012. Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113-116.
Albrechtsen, A., T. Sand Korneliussen, I. Moltke, T. van Overseem Hansen, F. C. Nielsen, and R. Nielsen. 2009. Relatedness mapping and tracts of relatedness for genome-wide data in the presence of linkage disequilibrium. Genet. Epidemiol. 33:266-274.
Albrechtsen, A., I. Moltke, and R. Nielsen. 2010. Natural selection and the distribution of Identity by descent in the human genome. Genetics 186:295-308.
Álvarez-Caballero, J. M., and E. Coy-Barrera. 2019. Chemical and antifungal variability of several accessions of Azadirachta indica A. Juss. from six locations across the Colombian Caribbean coast: identification of antifungal azadirone limonoids. Plants 8:555.
Akaike, H. 1974. A new look at the statistical model identification. IEEE Trans. Autom. Control 19:716-723.
Anderson, J. T., M. R. Wagner, C. A. Rushworth, K. V. S. K. Prasad, and T. Mitchell-Olds. 2014. The evolution of quantitative traits in complex environments. Heredity 112:4-12.
Andrews, S. 2010. FastQC: a quality control tool for high throughput sequence data. Available via http://www.bioinformatics.babraham.ac.uk/projects/fastqc.
Baldwin, I. T. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc. Natl. Acad. Sci. 95:8113-8118.
Bello-Bedoy, R., and J. Núñez-Farfán. 2010. Cost of inbreeding in resistance to herbivores in Datura stramonium. Ann. Bot. 105:747-753.
Berenbaum, M. R., A. R. Zangerl, and J. K. Nitao. 1986. Constraints on chemical coevolution: wild parsnips and the parsnip webworm. Evolution 40:1215-1228.
Bolger, A. M., M. Lohse, and B. Usadel. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120.
Browning, S. R., and B. L. Browning. 2012. Identity by descent between distant relatives: detection and applications. Annu. Rev. Genet. 46:617-633.
Castillo, G., L. L. Cruz, R. Tapia-López, E. Olmedo-Vicente, D. Carmona, A. L. Anaya-Lang, J. Fornoni, G. Andraca-Gómez, P. L. Valverde, and J. Núñez-Farfán. 2014. Selection mosaic exerted by specialist and generalist herbivores on chemical and physical defense of Datura stramonium. PLoS One 9:e102478.
Castells, E., M. A. Berhow, S. F. Vaughn, and M. R. Berenbaum. 2005. Geographic variation in alkaloid production in Conium maculatum populations experiencing differential herbivory by Agonopterix alstroemeriana. J. Chem. Ecol. 31:1693-1709.
Charlesworth, B. 1998. Measures of divergence between populations and the effect of forces that reduce variability. Mol. Biol. Evol. 15:538-543.
Chen, D., Q. Shao, L. Yin, A. Younis, and B. Zheng. 2018. Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front. Plant Sci. 9:1945.
Cogni, R., and D. J. Futuyma. 2009. Local adaptation in a plant herbivore interaction depends on the spatial scale. Biol. J. Linn. Soc. 97:494-502.
Daniels, R. F., S. F. Schaffner, E. A. Wenger, J. L. Proctor, H. H. Chang, W. Wong, N. Baro, D. Ndiaye, F. B. Fall, M. Ndiop, et al. 2015. Modeling malaria genomics reveals transmission decline and rebound in Senegal. Proc. Natl. Acad. Sci. 112:7067-7072.
Dawkins, R., and J. R. Krebs. 1979. Arms races between and within species. Proc. R. Soc. Lond. B Biol. Sci. 205:489-511.
De-la-Cruz, I. M., L. L. Cruz, L. Martínez-García, P. L. Valverde, C. M. Flores-Ortiz, L. B. Hernández-Portilla, and J. Núñez-Farfán. 2020. Evolutionary response to herbivory: population differentiation in microsatellite loci, tropane alkaloids and leaf trichome density in Datura stramonium. Arthropod Plant Interact. 14:21-30.
de Oliveira, D. A. B., A. V. da Silva, and E. dos Niculau. 2019. Molecular docking of azadirachtin in nuclear Ecdysone receptor. Curr. Phys. Chem. 6:50-57.
de Villemereuil, P., O. E. Gaggiotti, M. Mouterde, and I. Till-Bottraud. 2016. Common garden experiments in the genomic era: new perspectives and opportunities. Heredity 116:249-254.
Doyle, J. J., and J. L. Doyle. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19:11-15.
Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608.
Falconer, D. S., and T. Mackay. 1996. Introduction to quantitative genetics. Longmans Green, Harlow, U.K.
Flood, P. J., and A. M. Hancock. 2017. The genomic basis of adaptation in plants. Curr. Opin. Plant Biol. 36:88-94.
Fornoni, J., and J. Núñez-Farfán. 2000. Evolutionary ecology of Datura stramonium: genetic variation and costs for tolerance to defoliation. Evolution 54:789-797.
Fornoni, J., P. L. Valverde, and J. Núnez-Fárfan. 2004. Population variation in the cost and benefit of tolerance and resistance against herbivory in Datura stramonium. Evolution 58:1696-1704.
Gomulkiewicz, R., J. N. Thompson, R. D. Holt, S. L. Nuismer, and M. E. Hochberg. 2000. Hot spots, cold spots, and the geographic mosaic theory of coevolution. Am. Nat. 156:156-174.
Hahn, P. G., A. A. Agrawal, K. I. Sussman, and J. L. Maron. 2019. Population variation, environmental gradients, and the evolutionary ecology of plant defense against herbivory. Am. Nat 193:20-34.
Henden, L., S. Lee, I. Mueller, A. Barry, and M. Bahlo. 2018. Identity-by-descent analyses for measuring population dynamics and selection in recombining pathogens. PLos Genet 14:e1007279.
Janz, N. 2011. Ehrlich and Raven revisited: mechanisms underlying codiversification of plants and enemies. Annu. Rev. Ecol. Evol. Syst. 42:71-89.
Karban, R., and I. T. Baldwin. 2007. Induced responses to herbivory. Univ. of Chicago Press, Chicago.
Kariñho-Betancourt, E., A. A. Agrawal, R. Halitschke, and J. Núñez-Farfán. 2015. Phylogenetic correlations among chemical and physical plant defenses change with ontogeny. New Phytol. 206:796-806.
Kawecki, T. J., and D. Ebert. 2004. Conceptual issues in local adaptation. Ecol. Lett. 7:1225-1241.
Lande, R. 1979. Quantitative genetic analysis of multivariate evolution applied to brain: body size allometry. Evolution 33:402-416.
Lande, R., and S. J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226.
Li, H., and R. Durbin. 2009. Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 25:1754-1760.
Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, R. Durbin, and 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078-2079.
Lowry, D. B., J. T. Lovell, L. Zhang, J. Bonnette, P. A. Fay, R. B. Mitchell, J. Lloyd-Reilley, A. R. Boe, Y. Wu, F. M. Rouquette, et al. 2019. QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient. Proc. Natl. Acad. Sci. 116:12933-12941.
Martins, C. H. Z., B. P. Cunha, V. N. Solferini, and J. R. Trigo. 2015. Feeding on host plants with different concentrations and structures of pyrrolizidine alkaloids impacts the chemical-defense effectiveness of a specialist herbivore. PLoS One 10:e0141480.
Machado, B. B., J. P. M. Orue, M. S. Arruda, C. V. Santos, D. S. Sarath, W. N. Goncalves, G. G. Silva, H. Pistori, A. R. Roel, and J. F. Rodrigues-Jr. 2016. BioLeaf: a professional mobile application to measure foliar damage caused by insect herbivory. Comput. Electron. Agric. 129:44-55.
Mauricio, R., and M. D. Rausher. 1997. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51:1435-1444.
Miller, A. J., and W. F. Chamberlain. 1989. Azadirachtin as a larvicide against the horn fly, stable fly, and house fly (Diptera: Muscidae). J. Econ. Entomol. 82:1375-1378.
Miranda-Pérez, A., G. Castillo, J. Hernández-Cumplido, P. L. Valverde, M. Borbolla, L. L. Cruz, R. Tapia-López, J. Fornoni, C. M. Flores-Ortiz, and J. Núñez-Farfán. 2016. Natural selection drives chemical resistance of Datura stramonium. PeerJ 4:e1898.
Moore, B. D., R. L. Andrew, C. Külheim, and W. J. Foley. 2014. Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol. 201:733-750.
Motten, A. F., and J. Antonovics. 1992. Determinants of outcrossing rate in a predominantly self-fertilizing weed, Datura stramonium (Solanaceae). Am. J. Bot. 79:419-427.
Muola, A., P. Mutikainen, M. Lilley, L. Laukkanen, J.-P. Salminen, and R. Leimu. 2010. Associations of plant fitness, leaf chemistry, and damage suggest selection mosaic in plant-herbivore interactions. Ecology 91:2650-2659.
Núñez-Farfán, J., and R. Dirzo. 1994. Evolutionary ecology of Datura Stramonium L. in central Mexico: natural selection for resistance to herbivorous insects. Evolution 48:423-436.
Núnez-Farfán, J., R. A. Cabrales-Vargas, and R. Dirzo. 1996. Mating system consequences on resistance to herb ivory and life history traits in Datura stramonium. Am. J. Bot. 83:1041-1049.
Núñez-Farfán, J., J. Fornoni, and P. L. Valverde. 2007. The evolution of resistance and tolerance to herbivores. Annu. Rev. Ecol. Evol. Syst. 38:541-566.
Qamar, A., K. S. Mysore, and M. Senthil-Kumar. 2015. Role of proline and pyrroline-5-carboxylate metabolism in plant defense against invading pathogens. Front. Plant Sci. 6:503.
R Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Rastas, P. 2017. Lep-MAP3: robust linkage mapping even for low-coverage whole genome sequencing data. Bioinformatics 33:3726-3732.
Runquist Briscoe, R. D., A. J. Gorton, J. B. Yoder, N. J. Deacon, J. J. Grossman, S. Kothari, M. P. Lyons, S. N. Sheth, P. Tiffin, and D. A. Moeller. 2020. Context dependence of local adaptation to abiotic and biotic environments: a quantitative and qualitative synthesis. Am. Nat. 195:412-431.
Savolainen, O., M. Lascoux, and J. Merilä. 2013. Ecological genomics of local adaptation. Nat. Rev. Genet. 14:807-820.
Shonle, I., and J. Bergelson. 2000. Evolutionary ecology of the tropane alkaloids of Datura stramonium L. (Solanaceae). Evolution 54:778-788.
Sokal, R. R., and F. J. Rohlf. 1994. Biometry: the principles and practice of statistics in biological research. W H Freeman & Co, New York.
Stam, J. M., A. Kroes, Y. Li, R. Gols, J. J. A. van Loon, E. H. Poelman, and M. Dicke. 2014. Plant interactions with multiple insect herbivores: from community to genes. Annu. Rev. Plant Biol. 65:689-713.
Tamariz, J., E. Burgueño-Tapia, M. A. Vázquez, and F. Delgado. 2018. Pyrrolizidine alkaloids. Pp. 1-314 in H. J. Knölker, ed. The alkaloids: chemistry and biology. Vol. 80. Academic Press, Cambridge, MA.
Thompson, E. A. 2013. Identity by descent: variation in meiosis, across genomes, and in populations. Genetics 194:301-326.
Thompson, J. N. 2005. Coevolution: the geographic mosaic of coevolutionary arms races. Curr. Biol. 15:R992-R994.
Thompson, J. N., and B. M. Cunningham. 2002. Geographic structure and dynamics of coevolutionary selection. Nature 417:735-738.
Ujváry, I. 2010. Chapter 3-pest control agents from natural products. Pp. 119-229 in R. Krieger, ed. Hayes’ handbook of pesticide toxicology. 3rd ed. Academic Press, Cambridge, MA.
Valverde, P. L., J. Fornoni, and J. Núñez-Farfán. 2001. Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium. J. Evol. Biol. 14:424-432.
Valverde, P. L., J. Fornoni, and J. Núñez-Farfán 2003. Evolutionary ecology of Datura stramonium: equal plant fitness benefits of growth and resistance against herbivory. J. Evol. Biol. 16:127-137.
Verçosa, D., R. Cogni, M. N. Alves, and J. R. Trigo. 2019. The geographical and seasonal mosaic in a plant-herbivore interaction: patterns of defences and herbivory by a specialist and a non-specialist. Sci. Rep. 9:15206.
Wickham, H. 2016. ggplot2: elegant graphics for data analysis. 2nd ed. Springer International Publishing, Berlin, Germany.
Wise, M. J. 2009. Competition among herbivores of Solanum carolinense as a constraint on the evolution of host-plant resistance. Evol. Ecol. 23:347-361.
Wise, M. J. 2010. Diffuse interactions between two herbivores and constraints on the evolution of resistance in horsenettle (Solanum carolinense). Arthropod Plant Interact. 4:159-164.
Wise, M. J., and M. D. Rausher. 2013. Evolution of resistance to a multiple-herbivore community: genetic correlations, diffuse coevolution, and constraints on the plant's response to selection. Evolution 67:1767-1779.
Wittstock, U., and J. Gershenzon. 2002. Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr. Opin. Plant Biol. 5:300-307.
Wong, W., A. D. Griggs, R. F. Daniels, S. F. Schaffner, D. Ndiaye, A. K. Bei, A. B. Deme, B. MacInnis, S. K. Volkman, D. L. Hartl, et al. 2017. Genetic relatedness analysis reveals the cotransmission of genetically related Plasmodium falciparum parasites in Thiès, Senegal. Genome Med. 9:5.
Yamanaka, N., K. F. Rewitz, and M. B. O'Connor. 2013. Ecdysone control of developmental transitions: lessons from drosophila research. Annu. Rev. Entomol. 58:497-516.
Zar, J. H. 1999. Biostatistical analysis. Prentice Hall, Upper Saddle River, NJ.
Zhou, W., A. Kügler, E. McGale, A. Haverkamp, M. Knaden, H. Guo, F. Beran, F. Yon, R. Li, N. Lackus, et al. 2017. Tissue-specific emission of (E)-α-bergamotene helps resolve the dilemma when pollinators are also herbivores. Curr. Biol. 27:1336-1341.
Züst, T., C. Heichinger, U. Grossniklaus, R. Harrington, D. J. Kliebenstein, and L. A. Turnbull. 2012. Natural enemies drive geographic variation in plant defenses. Science 338:116-119.