Diversidad genética y variación fenotípica en una avispa parasitoide involucrada en la interacción entre yucas y sus polillas polinizadoras

Autores/as

  • C. Rocío Álamo-Herrera Centro de Investigación Científica y de Educación Superior de Ensenada
  • María Clara Arteaga Centro de Investigación Científica y de Educación Superior de Ensenada https://orcid.org/0000-0002-6647-4511
  • Rafael Bello-Bedoy Universidad Autónoma de Baja California

DOI:

https://doi.org/10.22201/ib.20078706e.2024.95.5461

Palabras clave:

Península de Baja California, Estructura genética, Asociación al hospedero, Morfometría, Interacción tri-trófica

Resumen

Las interacciones tritróficas entre plantas, herbívoros y parasitoides son un modelo valioso para estudiar cómo influyen en la distribución de la diversidad genética y la variabilidad fenotípica de las especies involucradas. Este estudio examinó la diversidad taxonómica, morfológica y genética de avispas parasitoides en la interacción Yucca-Tegeticula en la Península de Baja California. El estudio se realizó en 35 localidades recolectando 119 avispas parasitoides; 114 adultos y 5 pupas. Se identificaron 2 géneros de avispas: Bassus sp. (Ichneumonidae; n = 8) y Digonogastra sp. (Brachonidae; n = 111). Se encontraron niveles moderados de diversidad genética dentro de la población de Digonogastra en toda la península, constituyendo un único grupo panmítico con indicios de expansión demográfica histórica. Fenotípicamente, identificamos dimorfismo sexual y variación asociada con sus diferentes hospederos y la heterogeneidad ambiental a lo largo de la distribución geográfica de Digonogastra.

Citas

Abdala‐Roberts, L., Puentes, A., Finke, D. L., Marquis, R. J., Montserrat, M., Poelman, E. H. et al. (2019). Tri‐trophic interactions: bridging species, communities and ecosystems. Ecology Letters, 22, 2151–2167. https://doi.org/10.1111/ele.13392

Agrawal, A. A. (2001). Phenotypic plasticity in the interactions and evolution of species. Science, 294, 321–326. https://doi.org/10.1126/science.1060701

Althoff, D. M., & Thompson, J. N. (2001). Geographic structure in the searching behaviour of a specialist parasitoid: combining molecular and behavioural approaches. Journal of Evolutionary Biology, 14, 406–417. https://doi.org/10.1046/j.1420-9101.2001.00286.x

Althoff, D. M., Svensson, G. P., & Pellmyr, O. (2007). The influence of interaction type and feeding location on the phylogeographic structure of the yucca moth community associated with Hesperoyucca whipplei. Molecular Phylogenetics and Evolution, 43, 398–406. https://doi.org/10.1016/j.ympev.2006.10.015

Althoff, D. M. (2008). A test of host‐associated differentiation across the ‘parasite continuum’in the tri‐trophic interaction among yuccas, bogus yucca moths, and parasitoids. Molecular Ecology, 17, 3917–3927. https://doi.org/10.1111/j.1365-294X.2008.03874.x

Althoff, D. M., Segraves, K. A., Smith, C. I., Leebens-Mack, J., & Pellmyr, O. (2012). Geographic isolation trumps coevolution as a driver of yucca and yucca moth diversification. Molecular Phylogenetics and Evolution, 62, 898–906. https://doi.org/10.1016/j.ympev.2011.11.024

Althoff, D. M., & Segraves, K. A. (2022). Evolution of antagonistic and mutualistic traits in the yucca‐yucca moth obligate pollination mutualism. Journal of Evolutionary Biology, 35, 100–108. https://doi.org/10.1111/jeb.13967

Arteaga, M. C., Bello-Bedoy, R., & Gasca-Pineda, J. (2020). Hybridization between yuccas from Baja California: Genomic and environmental patterns. Frontiers in Plant Science, 11, 685. https://doi.org/10.3389/fpls.2020.00685

Baer, C. F., Tripp, D. W., Bjorksten, T. A., & Antolin, M. F. (2004). Phylogeography of a parasitoid wasp (Diaeretiella rapae): no evidence of host‐associated lineages. Molecular Ecology, 13, 1859–1869. https://doi.org/10.1111/j.1365-294X.2004.02196.x

Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

Carmona, D., Fitzpatrick, C. R., & Johnson, M. T. (2015). Fifty years of co‐evolution and beyond: integrating co‐evolution from molecules to species. Molecular Ecology, 24, 5315–5329. https://doi.org/10.1111/mec.13389

Crabb, B. A., & Pellmyr, O. (2006). Impact of the third trophic level in an obligate mutualism: do yucca plants benefit from parasitoids of yucca moths? International Journal of Plant Sciences, 167, 119–124. https://doi.org/10.1086/497844

Cuautle, M., & Rico‐Gray, V. (2003). The effect of wasps and ants on the reproductive success of the extrafloral nectaried plant Turnera ulmifolia (Turneraceae). Functional Ecology, 17, 417–423. https://doi.org/10.1046/j.1365-2435.2003.00732.x

Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772. https://doi.org/10.1038/nmeth.2109

Davidowitz, G., D’Amico, L. J., & Nijhout, H. F. (2004). The effects of environmental variation on a mechanism that controls insect body size. Evolutionary Ecology Research, 6, 49–62.

De la Rosa‐Conroy, L., Gasca‐Pineda, J., Bello‐Bedoy, R., Eguiarte, L. E., & Arteaga, M. C. (2020). Genetic patterns and changes in availability of suitable habitat support a colonization history of a North American perennial plant. Plant Biology, 22, 233–242. https://doi.org/10.1111/plb.13053

Ellers, J., & Jervis, M. (2003). Body size and the timing of egg production in parasitoid wasps. Oikos, 102, 164–172. https://doi.org/10.1034/j.1600-0706.2003.12285.x

Engelmann, G. (1872). The flower of yucca and its fertilization. Bulletin of the Torrey Botanical Club, 3, 33–33.

Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 2005, 47–50. https://doi.org/10.1177/117693430500100003

Folmer, O., Hoeh, W. R., Black, M. B., & Vrijenhoek, R. C. (1994). Conserved primers for PCR amplification of mitochondrial DNA from different invertebrate phyla. Molecular Marine Biology and Biotechnology, 3, 294–299.

Force, D. C., & Thompson, M. L. (1984). Parasitoids of the immature stages of several southwestern yucca moths. The Southwestern Naturalist, 29, 45–56. https://doi.org/10.2307/3670768

Garrick, R. C., Nason, J. D., Meadows, C. A., & Dyer, R. J. (2009). Not just vicariance: phylogeography of a Sonoran Desert euphorb indicates a major role of range expansion along the Baja peninsula. Molecular Ecology, 18, 1916–1931. https://doi.org/10.1111/j.1365-294X.2009.04148.x

Godfray, H. C. J. (1994). Parasitoids: behavioral and evolutionary ecology. New Jersey: Princeton University Press.

González-Abraham, C. E., Garcillán, P. P., & Ezcurra, E. (2010). Ecorregiones de la península de Baja California: una síntesis. Boletín de la Sociedad Botánica de México, 87, 69–82. https://doi:10.17129/botsci.302

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

Han, P., Desneux, N., Becker, C., Larbat, R., Le Bot, J., Adamowicz, S. et al. (2019). Bottom-up effects of irrigation, fertilization and plant resistance on Tuta absoluta: implications for Integrated Pest Management. Journal of Pest Science, 92, 1359–1370. https://doi.org/10.1007/s10340-018-1066-x

Harrington, S. M., Hollingsworth, B. D., Higham, T. E., & Reeder, T. W. (2018). Pleistocene climatic fluctuations drive isolation and secondary contact in the red diamond rattlesnake (Crotalus ruber) in Baja California. Journal of Biogeography, 45, 64–75. https://doi.org/10.1111/jbi.13114

Harrison, K., Tarone, A. M., DeWitt, T., & Medina, R. F. (2022). Predicting the occurrence of host‐associated differentiation in parasitic arthropods: a quantitative literature review. Entomologia Experimentalis et Applicata, 170, 5–22. https://doi.org/10.1111/eea.13123

Hebert, P. D., Ratnasingham, S., Zakharov, E. V., Telfer, A. C., Levesque-Beaudin, V., Milton, M. A. et al. (2016). Counting animal species with DNA barcodes: Canadian insects. Philosophical Transactions of the Royal Society B: Biological Sciences, 371, 20150333. https://doi.org/10.1098/rstb.2015.0333

Heil, M. (2008). Indirect defence via tritrophic interactions. New Phytologist, 178, 41–61. https://doi.org/10.1111/j.1469-8137.2007.02330.x

Hufbauer, R. A., Bogdanowicz, S. M., & Harrison, R. G. (2004). The population genetics of a biological control introduction: mitochondrial DNA and microsatellie variation in native and introduced populations of Aphidus ervi, a parisitoid wasp. Molecular Ecology, 13, 337–348. https://doi.org/10.1046/j.1365-294X.2003.02084.x

Hurlbutt, B. (1987). Sexual size dimorphism in parasitoid wasps. Biological Journal of the Linnean Society, 30, 63–89. https://doi.org/10.1111/j.1095-8312.1987.tb00290.x

Jervis, M. A., Ellers, J., & Harvey, J. A. (2008). Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annual Review of Entomology, 53, 361–385. https://doi.org/10.1146/annurev.ento.53.103106.093433

Kankare, M., Van Nouhuys, S., & Hanski, I. (2005). Genetic divergence among host-specific cryptic species in Cotesia melitaearum aggregate (Hymenoptera: Braconidae), parasitoids of checkerspot butterflies. Annals of the Entomological Society of America, 98, 382–394. https://doi.org/10.1603/0013-8746(2005)098[0382:GDAHCS]2.0.CO;2

Kappers, I. F., Hoogerbrugge, H., Bouwmeester, H. J., & Dicke, M. (2011). Variation in herbivory-induced volatiles among cucumber (Cucumis sativus L.) varieties has consequences for the attraction of carnivorous natural enemies. Journal of Chemical Ecology, 37, 150–160. https://doi.org/10.1007/s10886-011-9906-7

Karns, G. (2009). Genetic differentiation of the parasitoid, Cotesia congregata (Say), based on host-plant complex (M. Sc. Thesis). Virginia Commonwealth University. VA, USA. https://doi.org/10.25772/1E5V-N037

Lenz, L. W. (1998). Yucca capensis (Agavaceae, Yuccoideae), a new species from Baja California Sur, Mexico. Cactus and Succulent Journal, 70, 289–296.

Lozier, J. D., Roderick, G. K., & Mills, N. J. (2009). Molecular markers reveal strong geographic, but not host associated, genetic differentiation in Aphidius transcaspicus, a parasitoid of the aphid genus Hyalopterus. Bulletin of Entomological Research, 99, 83–96. https://doi.org/10.1017/S0007485308006147

Mazer, S. J., & Damuth, J. (2001). Nature and causes of variation. In C. W. Fox, D. A. Roff, & D. J. Fairbairn (Ed). Evolutionary ecology: concepts and case studies (pp. 3–15). Oxford, UK: Oxford University Press.

Nason, J. D., Hamrick, J. L., & Fleming, T. H. (2002). Historical vicariance and postglacial colonization effects on the evolution of genetic structure in Lophocereus, a Sonoran Desert columnar cactus. Evolution, 56, 2214–2226. https://doi.org/10.1111/j.0014-3820.2002.tb00146.x

Navascués, M., Vaxevanidou, Z., González-Martínez, S. C., Climent, J., Gil, L., & Emerson, B. C. (2006). Chloroplast microsatellites reveal colonization and metapopulation dynamics in the Canary Island pine. Molecular Ecology, 15, 2691–2698. https://doi.org/10.1111/j.1365-294X.2006.02960.x

Nei, M., & Li, W. H. (1979). Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences, 76, 5269–5273. https://doi.org/10.1073/pnas.76.10.5269

Nei, M. (1987). Molecular evolutionary genetics. New York: Columbia University Press.

Pekas, A., & Wäckers, F. L. (2020). Bottom-up effects on tri-trophic interactions: Plant fertilization enhances the fitness of a primary parasitoid mediated by its herbivore host. Journal of Economic Entomology, 113, 2619–2626. https://doi.org/10.1093/jee/toaa204

Pellmyr, O., & Leebens-Mack, J. (1999). Forty million years of mutualism: evidence for Eocene origin of the yucca-yucca moth association. Proceedings of the National Academy of Sciences, 96, 9178–9183. https://doi.org/10.1073/pnas.96.16.9178

Pellmyr, O. (2003). Yuccas, yucca moths, and coevolution: a review. Annals of the Missouri Botanical Garden, 90, 35–55. https://doi.org/10.2307/3298524

Pigliucci, M. (2003). Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecology Letters, 6, 265–272. https://doi.org/10.1046/j.1461-0248.2003.00428.x

Powell, J. A. (1989). Synchronized, mass-emergences of a yucca moth, Prodoxus Y-inversus (Lepidoptera: Prodoxidae), after 16 and 17 years in diapause. Oecologia, 81, 490–493. https://doi.org/10.1007/BF00378957

Quicke, D. L. (2015). The Braconid and Ichneumonid parasitoid wasps: Biology, Systematics, Evolution and Ecology. Metopiinae. Oxford: Wiley Blackwell.

Resh, V. H., & Cardé, R. T. (Eds.). (2009). Encyclopedia of insects. San Diego, CA: Academic press.

Roderick, G. K. (1996). Geographic structure of insect populations: gene flow, phylogeography, and their uses. Annual Review of Entomology, 41, 325–352. https://doi.org/10.1146/annurev.en.41.010196.001545

Rogers, A. R., & Harpending, H. (1992). Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552–569. https://doi.org/10.1093/oxfordjournals.molbev.a040727

Rozas, J., Sánchez-DelBarrio, J. C., Messeguer, X., & Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496–2497. https://doi.org/10.1093/bioinformatics/btg359

Sánchez, J. A., Romero, J., Ramírez, S., Anaya, S., & Carrillo, J. L. (1998). Géneros de Braconidae del estado de Guanajuato (Insecta: Hymenoptera). Acta Zoológica Mexicana (nueva serie), 79, 59–137. https://doi.org/10.21829/azm.1998.74741721

Sarfraz, M., Dosdall, L. M., & Keddie, B. A. (2009). Host plant nutritional quality affects the performance of the parasitoid Diadegma insulare. Biological Control, 51, 34–41. https://doi.org/10.1016/j.biocontrol.2009.07.004

Schoonhoven, L. M., Van Loon, J. J., & Dicke, M. (2005). Insect-plant biology. Oxford: Oxford University Press.

Seifert, C. L., Strutzenberger, P., & Fiedler, K. (2022). Ecological specialisation and range size determine intraspecific body size variation in a speciose clade of insect herbivores. Oikos, 2022, e09338. https://doi.org/10.1111/oik.09338

Singer, M. S., & Stireman III, J. O. (2005). The tri‐trophic niche concept and adaptive radiation of phytophagous insects. Ecology Letters, 8, 1247–1255. https://doi.org/10.1111/j.1461-0248.2005.00835.x

Stillwell, R. C., & Fox, C. W. (2007). Environmental effects on sexual size dimorphism of a seed-feeding beetle. Oecologia, 153, 273–280. https://doi.org/10.1007/s00442-007-0724-0

Stillwell, R. C., & Fox, C. W. (2009). Geographic variation in body size, sexual size dimorphism and fitness components of a seed beetle: local adaptation versus phenotypic plasticity. Oikos, 118, 703–712. https://doi.org/10.1111/j.1600-0706.2008.17327.x

StiremanIII, J. O., Nason, J. D., & Heard, S. B. (2005). Host‐associated genetic differentiation in phytophagous insects: general phenomenon or isolated exceptions? Evidence from a goldenrod‐insect community. Evolution, 59, 2573–2587. https://doi.org/10.1111/j.0014-3820.2005.tb00970.x

Takabayashi, J., & Dicke, M. (1996). Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends in plant science, 1, 109–113. https://doi.org/10.1016/S1360-1385(96)90004-7

Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599. https://doi.org/10.1093/molbev/msm092

Turner, R. M., Bowers, J. E., & Brugess, T. L. (2022). Sonoran Desert plants: an ecological atlas. Tucson: University of Arizona Press.

Vilhelmsen, L., Isidoro, N., Romani, R., Basibuyuk, H. H., & Quicke, D. L. (2001). Host location and oviposition in a basal group of parasitic wasps: the subgenual organ, ovipositor apparatus and associated structures in the Orussidae (Hymenoptera, Insecta). Zoomorphology, 121, 63–84. https://doi.org/10.1007/s004350100046

Visser, M. E. (1994). The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). Journal of Animal Ecology, 963–978. https://doi.org/10.2307/5273

Wonglersak, R., Fenberg, P. B., Langdon, P. G., Brooks, S. J., & Price, B. W. (2020). Temperature‐body size responses in insects: a case study of British Odonata. Ecological Entomology, 45, 795–805. https://doi.org/10.1111/een.12853

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Publicado

2024-10-21

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ECOLOGÍA