Phenotypic selection gradients in a tripartite plant interaction in southern South America
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
Consejo Nacional de Investigaciones Científicas y Técnicas
Fondo para la Investigación Científica y Tecnológica
GRFT 2019
Ministerio de Ciencia y Tecnología del Gobierno de Córdoba
PubMed
40829660
PubMed Central
PMC12364580
DOI
10.1098/rspb.2025.1182
Knihovny.cz E-zdroje
- Klíčová slova
- arbuscular mycorrhizal fungi, hawkmoth pollinators, herbivores, natural selection, urbanization,
- MeSH
- býložravci MeSH
- ekosystém MeSH
- fenotyp MeSH
- mykorhiza * fyziologie MeSH
- opylení MeSH
- selekce (genetika) * MeSH
- symbióza * MeSH
- Publikační typ
- časopisecké články MeSH
The study of how phenotypic selection by plant mutualists and antagonists varies within ecosystems is crucial for evaluating potential plant adaptations to changing environments, such as urban areas. Here, we describe the interaction intensity of plants with their mutualistic and antagonistic partners, as well as the selective landscapes in one natural and one urban site. We measured direct phenotypic selection on plant traits relevant to three interaction partners: floral tube length, resistance to herbivores and arbuscular mycorrhizal fungi (AMF) colonization. Significant direct phenotypic selection on the three interaction traits was detected in the natural site. We observed disruptive selection on floral tube length, with the two fitness optima closely matching the proboscis peak lengths of the main pollinator species. In addition, we observed stabilizing selection by arbuscular mycorrhizal fungi, favouring plants with around 11% of arbuscular colonization. This result supports the idea that plants may autoregulate mean intraradical arbuscular colonization to maximize fitness relative to carbon allocation to arbuscular mycorrhizal fungi. Finally, we detected directional selection benefiting plants with high resistance to herbivores. Our results highlight the importance of adopting a multispecies, context-dependent approach to better understand the complex ecological interactions that drive plant evolution.
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Strauss SY, Irwin RE. 2004. Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu. Rev. Ecol. Evol. Syst. 35, 435–466. ( 10.1146/annurev.ecolsys.35.112202.130215) DOI
Barrett SCH, Harder LD. 1996. Ecology and evolution of plant mating. Trends Ecol. Evol. 11, 73–79. ( 10.1016/0169-5347(96)81046-9) PubMed DOI
Smith SE, Read D. 2008. Mycorrhizal symbiosis, p. 815. London: Academic Press.
Strauss SY, Agrawal AA. 1999. The ecology and evolution of plant tolerance to herbivory. Trends Ecol. Evol. 14, 179–185. ( 10.1016/s0169-5347(98)01576-6) PubMed DOI
Irwin RE, Warren PS, Adler LS. 2018. Phenotypic selection on floral traits in an urban landscape. Proc. R. Soc. B 285, 20181239. ( 10.1098/rspb.2018.1239) PubMed DOI PMC
Brodie ED, Moore AJ, Janzen FJ. 1995. Visualizing and quantifying natural selection. Trends Ecol. Evol. 10, 313–318. ( 10.1016/s0169-5347(00)89117-x) PubMed DOI
Charmantier A, Burkhard T, Gervais L, Perrier C, Schulte‐Hostedde AI, Thompson MJ. 2024. How does urbanization affect natural selection? Funct. Ecol. 38, 2522–2536. ( 10.1111/1365-2435.14667) DOI
Benkman CW. 2013. Biotic interaction strength and the intensity of selection. Ecol. Lett. 16, 1054–1060. ( 10.1111/ele.12138) PubMed DOI
Cocucci AA, Moré M, Sérsic A, More M, Sersic AN. 2009. Restricciones mecánicas en las interacciones planta-polinizador: estudios de caso en plantas polinizadas por esfíngidos. In Ecología y evolución de interacciones planta-animal (eds Medel R, Aizen MA, Zamora R), pp. 43–59. Santiago, Chile: Editorial Universitaria.
Haverkamp A, Hansson BS, Baldwin IT, Knaden M, Yon F. 2018. Floral trait variations among wild tobacco populations influence the foraging behavior of hawkmoth pollinators. Front. Ecol. Evol. 6, 1–10. ( 10.3389/fevo.2018.00019) DOI
Haxaire J. 2019. A revised and annotated checklist of the Brazilian Sphingidae with new records, taxonomical notes, and description of one new species (Lepidoptera Sphingidae). In Eur entomol pp. 101–187
Kitching IJ. 2022. Sphingidae Taxonomic Inventory. See http://sphingidae.myspecies.info/.
Izaguirre MM, Mazza CA, Svatos A, Baldwin IT, Ballaré CL. 2007. Solar ultraviolet-B radiation and insect herbivory trigger partially overlapping phenolic responses in Nicotiana attenuata and Nicotiana longiflora. Ann. Bot. 99, 103–109. ( 10.1093/aob/mcl226) PubMed DOI PMC
Montero GA. 2014. Ecología de las interacciones entre malezas y artrópodos. In Capítulo x. malezas e invasoras argent ecol manejo, p. 964, vol. 1.
Fornoni J, Valverde PL, Núñez-Farfán J. 2004. Population variation in the cost and benefit of tolerance and resistance against herbivory in Datura stramonium. Evolution (N Y) 58, 1696–1704. ( 10.1111/j.0014-3820.2004.tb00455.x) PubMed DOI
Rausher MD, Simms EL. 1989. The Evolution of Resistance to Herbivory in Ipomoea Purpurea. I. Attempts to Detect Selection. Evolution 43, 563–572. ( 10.2307/2409059) PubMed DOI
Marro N, et al. 2022. The effects of arbuscular mycorrhizal fungal species and taxonomic groups on stressed and unstressed plants: a global meta‐analysis. New Phytol. 235, 320–332. ( 10.1111/nph.18102) PubMed DOI
Hoeksema JD. 2010. Ongoing coevolution in mycorrhizal interactions. New Phytol. 187, 286–300. ( 10.1111/j.1469-8137.2010.03305.x) PubMed DOI
Gutjahr C. 2014. Phytohormone signaling in arbuscular mycorhiza development. Curr. Opin. Plant Biol. 20, 26–34. ( 10.1016/j.pbi.2014.04.003) PubMed DOI
Chaudhary VB, et al. 2022. What are mycorrhizal traits? Trends Ecol. Evol. 37, 573–581. ( 10.1016/j.tree.2022.04.003) PubMed DOI
Lehnert H, Serfling A, Enders M, Friedt W, Ordon F. 2017. Genetics of mycorrhizal symbiosis in winter wheat (Triticum aestivum). New Phytol. 215, 779–791. ( 10.1111/nph.14595) PubMed DOI
Chialva M, Stelluti S, Novero M, Masson S, Bonfante P, Lanfranco L. 2024. Genetic and functional traits limit the success of colonisation by arbuscular mycorrhizal fungi in a tomato wild relative. Plant Cell Environ. 47, 4275–4292. ( 10.1111/pce.15007) PubMed DOI
Rúa MA, Hoeksema JD. 2024. Interspecific selection in a diverse mycorrhizal symbiosis. Sci. Rep. 14, 12151. ( 10.1038/s41598-024-62815-4) PubMed DOI PMC
Wang C, Reid JB, Foo E. 2018. The Art of Self-Control – Autoregulation of Plant–Microbe Symbioses. Front. Plant Sci. 9, 1–8. ( 10.3389/fpls.2018.00988) PubMed DOI PMC
Fugère V, Hendry AP. 2018. Human influences on the strength of phenotypic selection. Proc. Natl Acad. Sci. USA 115, 10070–10075. ( 10.1073/pnas.1806013115) PubMed DOI PMC
Lahti DC, Johnson NA, Ajie BC, Otto SP, Hendry AP, Blumstein DT, Coss RG, Donohue K, Foster SA. 2009. Relaxed selection in the wild. Trends Ecol. Evol. 24, 487–496. ( 10.1016/j.tree.2009.03.010) PubMed DOI
Ashman TL, et al. 2004. Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408–2421. ( 10.1890/03-8024) DOI
Ushimaru A, Kobayashi A, Dohzono I. 2014. Does urbanization promote floral diversification? Implications from changes in herkogamy with pollinator availability in an urban-rural area. Am. Nat. 184, 258–267. ( 10.1086/676855) PubMed DOI
López-Ráez JA. 2016. How drought and salinity affect arbuscular mycorrhizal symbiosis and strigolactone biosynthesis? Planta 243, 1375–1385. ( 10.1007/s00425-015-2435-9) PubMed DOI
Thompson MJ, Capilla-Lasheras P, Dominoni DM, Réale D, Charmantier A. 2022. Phenotypic variation in urban environments: mechanisms and implications. Trends Ecol. Evol. 37, 171–182. ( 10.1016/j.tree.2021.09.009) PubMed DOI
Figueroa-Castro DM, Holtsford TP. 2009. Post-pollination mechanisms in Nicotiana longiflora and N. plumbaginifolia: pollen tube growth rate, offspring paternity and hybridization. Sex. Plant Reprod. 22, 187–196. PubMed
Cabido M, Zeballos SR, Zak M, Carranza ML, Giorgis MA, Cantero JJ, Acosta ATR. 2018. Native woody vegetation in central Argentina: Classification of Chaco and Espinal forests. Appl. Veg. Sci. 21, 298–311. ( 10.1111/avsc.12369) DOI
Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675. ( 10.1038/nmeth.2089) PubMed DOI PMC
Phillips JM, Hayman DS. 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55, 158–161. ( 10.1016/s0007-1536(70)80110-3) DOI
Grace C, Stribley DP. 1991. A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol. Res. 95, 1160–1162. ( 10.1016/s0953-7562(09)80005-1) DOI
McGonigle TP, Miller M, Evans DG, Fairchild GL, Swan JA, Road O. 1990. A method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol. 115, 495–501. PubMed
Walker C, Mize CW, McNabb HS. 1982. Populations of endogonaceous fungi at two locations in central Iowa. Can. J. Bot. 60, 2518–2529. ( 10.1139/b82-305) DOI
Omar MB, Bolland L, Heather WA. 1979. A permanent mounting medium for fungi. Bull. Br. Mycol. Soc. 13, 31–32. ( 10.1016/s0007-1528(79)80038-3) PubMed DOI
Oehl F, Sieverding E, Palenzuela J, Ineichen K, da Silva GA. 2011. Advances in Glomeromycota taxonomy and classification. IMA Fungus 2, 191–199. ( 10.5598/imafungus.2011.02.02.10) PubMed DOI PMC
Barber NA, Soper Gorden NL. 2015. How do belowground organisms influence plant-pollinator interactions? Journal of Plant Ecology 8, 1–11. ( 10.1093/jpe/rtu012) DOI
Munguía-Rosas MA, Arias LM, Jurado-Dzib SG, Mezeta-Cob CR, Parra-Tabla V. 2015. Effects of herbivores and pollinators on fruit yield and survival in a cleistogamous herb. Plant Ecol. 216, 517–525. ( 10.1007/s11258-015-0455-y) DOI
Adler LS, Wink M, Distl M, Lentz AJ. 2006. Leaf herbivory and nutrients increase nectar alkaloids. Ecol. Lett. 9, 960–967. ( 10.1111/j.1461-0248.2006.00944.x) PubMed DOI
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM. 2009. Mixed effects models and extensions in ecology with R. In Statistics for biology and health (eds Gail M, Krickeberg K, Samet JM, Tsiatis A, Wong W), p. 574, vol. 32. New York, NY: Springer New York. ( 10.1007/978-0-387-87458-6) DOI
Lande R, Arnold SJ. 1983. The measurement of selection on correlated characters. Evolution 37, 1210–1226. ( 10.1111/j.1558-5646.1983.tb00236.x) PubMed DOI
Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–51. ( 10.18637/jss.v067.i01) DOI
R Core Team . 2025. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See https://www.R-project.org/.
Wood SN. 2017. Generalized additive models. New York: Chapman Hall/CRC. See https://www.taylorfrancis.com/books/9781498728348.
Wood SN. 2008. Fast stable direct fitting and smoothness selection for generalized additive models. J. R. Stat. Soc. Ser. B Sat. Methodol. 70, 495–518. ( 10.1111/j.1467-9868.2007.00646.x) DOI
Ali JG, Agrawal AA. 2012. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17, 293–302. ( 10.1016/j.tplants.2012.02.006) PubMed DOI
Carmona D, Fornoni J. 2013. Herbivores can select for mixed defensive strategies in plants. New Phytol. 197, 576–585. ( 10.1111/nph.12023) PubMed DOI
Reinhardt D. 2007. Programming good relations–development of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 10, 98–105. ( 10.1016/j.pbi.2006.11.001) PubMed DOI
Chagnon PL, Bradley RL, Maherali H, Klironomos JN. 2013. A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci. 18, 484–491. ( 10.1016/j.tplants.2013.05.001) PubMed DOI
Davison J, et al. 2020. Plant functional groups associate with distinct arbuscular mycorrhizal fungal communities. New Phytol. 226, 1117–1128. ( 10.1111/nph.16423) PubMed DOI
García de León D, et al. 2018. Anthropogenic disturbance equalizes diversity levels in arbuscular mycorrhizal fungal communities. Glob. Chang. Biol. 24, 2649–2659. ( 10.1111/gcb.14131) PubMed DOI
Frew A, Antunes PM, Cameron DD, Hartley SE, Johnson SN, Rillig MC, Bennett AE. 2022. Plant herbivore protection by arbuscular mycorrhizas: a role for fungal diversity? New Phytol. 233, 1022–1031. ( 10.1111/nph.17781) PubMed DOI
Chen K, Kleijn D, Scheper J, Fijen TPM. 2022. Additive and synergistic effects of arbuscular mycorrhizal fungi, insect pollination and nutrient availability in a perennial fruit crop. Agric. Ecosyst. Environ. 325, 107742. ( 10.1016/j.agee.2021.107742) DOI
Gange AC, Smith AK. 2005. Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects. Ecol. Entomol. 30, 600–606. ( 10.1111/j.0307-6946.2005.00732.x) DOI
Rodewald AD, Arcese P. 2017. Reproductive Contributions of Cardinals Are Consistent with a Hypothesis of Relaxed Selection in Urban Landscapes. Front. Ecol. Evol. 5. ( 10.3389/fevo.2017.00077) DOI
Straka TM52, von der Lippe M, Voigt CC, Gandy M, Kowarik I, Buchholz S. 2021. Light pollution impairs urban nocturnal pollinators but less so in areas with high tree cover. Sci. Total Environ. 778, 146244. ( 10.1016/j.scitotenv.2021.146244) PubMed DOI
Bariles JB, Cocucci AA, Soteras F. 2021. Pollination and fitness of a hawkmoth-pollinated plant are related to light pollution and tree cover. Biological Journal of the Linnean Society 134, 815–822. ( 10.1093/biolinnean/blab114) DOI
Day Briggs S, Anderson JT. 2025. The effect of global change on the expression and evolution of floral traits. Ann. Bot. 135, 9–24. ( 10.1093/aob/mcae057) PubMed DOI PMC
Soteras F. 2025. Data and code from: Phenotypic selection on plant mycorrhizal, leaf, and floral traits is relaxed in an urbanization context. Zenodo. ( 10.5281/zenodo.14714462) DOI
Soteras F, et al. 2025. Supplementary material from: Phenotypic selection gradients in a tripartite plant interaction in southern South America. Figshare. ( 10.6084/m9.figshare.c.7958567) PubMed DOI
Phenotypic selection gradients in a tripartite plant interaction in southern South America