Tasty rewards for ants: differences in elaiosome and seed metabolite profiles are consistent across species and reflect taxonomic relatedness
- 261 Downloads
Diaspores of myrmecochorous plants consist of a seed (or fruit) and an attached appendage (elaiosome) which attracts ants. The elaiosome is a food resource for ants, whereas the seed is an energy source for subsequent germination and plant establishment. Although myrmecochory occurs in many phylogenetically unrelated lineages, multiple phylogenetic lineages display similar variation in elaiosome and seed metabolite composition due to convergent evolution. We focused on four families (Amaryllidaceae, Boraginaceae, Papaveraceae and Poaceae) each represented by two species from different genera. Diaspores of three populations per species were sampled and concentrations of 60 metabolites from five groups (amino acids, fatty acids, organic acids, polyols and sugars) were determined for both elaiosomes and seeds. Variability in metabolite composition was decomposed by hierarchical ANOVA and variation partitioning using redundancy analysis (reflecting both species nested within families, crossed with seed vs. elaiosome). Differences in the metabolite composition of elaiosomes and seeds were consistent across multiple phylogenetic origins (with more pronounced differences at the level of individual metabolites than at the level of metabolite groups) and supported the idea of convergent evolution under strong selection pressure. Elaiosomes contained higher amounts of easily digestible metabolites (especially amino acids) than seeds. Fatty acids were not more concentrated in elaiosomes, which contradicts the literal translation of “elaiosome” (= oil body). The differentiation of metabolite composition closely reflected taxonomic relatedness, particularly at the family level. Differences among populations within species were small, so the metabolite composition can thus be considered as a trait with relatively low intraspecific variability.
KeywordsMyrmecochory Convergent evolution Variation partitioning Ant–plant mutualism Seed dispersal
Anna Heydova is gratefully acknowledged for skilled analytical sample preparation, Conor Redmond for editing our English and Pavel Fibich for the help with drawing figures in R. The research was supported by the Czech Science Foundation—GACR 14-36079G—PLADIAS.
Author contribution statement
MK and JL designed the experiment, MK collected the plant diaspores and prepared separated samples of elaisomes and seeds, MM and HZ conducted the chemical analyses, MK and JL carried out the statistical analyses. MK wrote the first draft of the manuscript with JL, and MM, HZ and PŠ contributed the chemical aspects. All the authors revised the text and agreed upon the final version.
- Bresinsky A (1963) Bau, Entwicklungsgeschichte und Inhaltsstoffe der Elaiosomen. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, pp 1–54Google Scholar
- Bresinsky A (2014) Ants, plants and fungi: a view on some patterns of interaction and diversity. In: Lüttge U, Beyschlag W, Progress in botany 75. Springer-Verlag, Berlin Heidelberg, pp 3–54. https://doi.org/10.1007/978-3-642-38797-5_1Google Scholar
- Dunn RR, Gove AD, Barraclough TG, Givnish TJ, Majer JD (2007) Convergent evolution of an ant–plant mutualism across plant families, continents, and time. Evol Ecol Res 9:1349–1362Google Scholar
- Košťál V, Doležal R, Rozsypal J, Moravcová M, Zahradníčková H, Šimek P (2011a) Physiological and biochemical analysis of overwintering and cold tolerance in two Central European populations of the spruce bark beetle, Ips typographus. J Insect Physiol 57:1136–1146. https://doi.org/10.1016/j.jinsphys.2011.03.011 CrossRefPubMedGoogle Scholar
- Mayer V, Svoma E (1998) Development and function of the elaiosome in Knautia (Dipsacaceae). Bot Acta 111:402–410. https://doi.org/10.1111/j.1438-8677.1998.tb00726.x CrossRefGoogle Scholar
- Mayer V, Ölzant S, Fischer RC (2005) Myrmecochorous seed dispersal in temperate regions. In: Forget PM, Lambert JE, Hulme PE, Vander Wall SB (eds) Seed fate predation, dispersal and seedling establishment. CABI Publishing, Wallingford, p 175–196Google Scholar
- Schmeer K, Nicholson G, Zhang S, Bayer E, Bohning-Gaese K (1996) Identification of the lipids and the ant attractant 1,2-dioleolglycerol in the arils of Commiphora guillaumini Perr. (Burseraceae) by supercritical fluid chromatography-atmospheric pressure chemical ionisation mass spektrometry. J Chromatogr 727:139–146CrossRefGoogle Scholar
- Sernander R (1906) Entwurf einer Monographie der europäischen Myrmekochoren. Kungliga Svenska Vetenskapsakademiens Handlingar 41:1–410Google Scholar
- Šmilauer P, Lepš J (2014) Multivariate analysis of ecological data using Canoco 5. Cambridge University Press, Cambridge, pp 1–362. https://doi.org/10.1017/cbo9781139627061Google Scholar
- Stevens PF (2016) Angiosperm Phylogeny Website. Version 13. http://www.mobot.org/MOBOT/research/APweb/. Accessed 4 Sept 2016
- ter Braak CJF, Šmilauer P (2012) CANOCO Reference manual and User´s guide: Software for ordination (version 5.0). Microcomputer Power, Ithaca, pp 1–496Google Scholar
- Zahradníčková H, Tomčala A, Berková P, Schneedorferová I, Okrouhlík J, Šimek P, Hodková M (2014) Cost effective, robust, and reliable coupled separation techniques for the identification and quantification of phospholipids in complex biological matrices: application to insects. J Sep Sci 37:2062–2068. https://doi.org/10.1002/jssc.201400113 CrossRefPubMedGoogle Scholar