Abstract
The outcome of interspecific competition is affected by numerous abiotic and biotic factors. However, the effects of genetic relatedness of conspecific neighbours have not been elucidated. Here, we demonstrate that the genotype of a conspecific neighbour determines the outcome of interspecific competition. We investigated effects of genotype of neighbour sibling or non-sibling Plantago asiatica plants on competition with Trifolium repens plants. Pairs of P. asiatica, sibling or non-sibling, were grown in competition with T. repens. Sibling P. asiatica plants, but not non-sibling plants, increased leaf placement towards competitor T. repens plants, and that placement was correlated negatively with the biomass of T. repens and positively with seed production by P. asiatica. Seed production by P. asiatica plants competing with T. repens was greater in individuals paired with siblings than in those paired with non-siblings. Thus, our results show that the genotype of conspecific neighbours can alter the outcome of interspecific competition.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data are available in the main text or the supplementary materials.
References
Aarssen LW (2015) Body size and fitness in plants: revisiting the selection consequences of competition. Perspect Plant Ecol Evol Syst 17:236–242. https://doi.org/10.1016/j.ppees.2015.02.004
Argyle M (2013) Cooperation: The basis of sociability. (Routledge), New York. https://doi.org/10.4324/9780203786758
Argyres AZ, Schmitt J (1991) Microgeographic genetic structure of morphological and life history traits in a natural population of Impatiens capensis. Evolution 45:178–189. https://doi.org/10.1111/j.1558-5646.1991.tb05276.x
Badri DV, De-la-Peña C, Lei Z, Manter DK, Chaparro JM, Guimarães RL, Sumner LW, Vivanco JM (2012) Root screted metabolites and proteins are involved in the early events of plant-plant recognition prior to competition. PLoS ONE 7:e46640. https://doi.org/10.1371/journal.pone.0046640
Baron E, Richirt J, Villoutreix R, Amsellem L, Roux F (2015) The genetics of intra- and interspecific competitive response and effect in a local population of an annual plant species. Funct Ecol 29:1361–1370. https://doi.org/10.1111/1365-2435.12436
Biedrzycki ML, Jilany TA, Dudley SA, Bais HP (2010) Root exudates mediate kin recognition in plants. Commun Integr Biol 3:28–35. https://doi.org/10.4161/cib.3.1.10118
Biernaskie JM (2011) Evidence for competition and cooperation among climbing plants. Proc R Soc B 278:1989–1996. https://doi.org/10.1098/rspb.2010.1771
Bonser SP (2013) High reproductive efficiency as an adaptive strategy in competitive environments. Funct Ecol 27:876–885. https://doi.org/10.1111/1365-2435.12064
Craine JM, Dybzinski R (2013) Mechanisms of plant competition for nutrients, water and light. Funct Ecol 27:833–840. https://doi.org/10.1111/1365-2435.12081
Crepy M, Casal JJ (2015) Photoreceptor-mediated kin recognition in plants. New Phytol 205:329–338. https://doi.org/10.1111/nph.13040
de Wit M, Kegge W, Evers JB, Vergeer-van Eijk MH, Gankema P, Voesenek LACJ, Pierik R (2012) Plant neighbor detection through touching leaf tips precedes phytochrome signals. Proc Natl Acad Sci USA 109:14705–14710. https://doi.org/10.1073/pnas.1205437109
Dudley SA, File AL (2007) Kin recognition in an annual plant. Biol Lett 3:435–438. https://doi.org/10.1098/rsbl.2007.0232
Dudley SA, Murphy GP, File AL (2013) Kin recognition and competition in plants. Funct Ecol 27:898–906. https://doi.org/10.1111/1365-2435.12121
Ehlers BK, David P, Damgaard CF, Lenormand T (2016) Competitor relatedness, indirect soil effects, and plant coexistence. J Ecol 104:1126–1135. https://doi.org/10.1111/1365-2745.12568
Hamilton WD (1964a) The genetical evolution of social behaviour. I. Theol Biol 7:1–16. https://doi.org/10.1016/0022-5193(64)90038-4
Hamilton WD (1964b) The genetical evolution of social behaviour. II. Theol Biol 7:17–52. https://doi.org/10.1016/0022-5193(64)90039-6
Karban R, Shiojiri K, Ishizaki S, Wetzel WC, Evans RY (2013) Kin recognition affects plant communication and defence. Proc R Soc B 280:20123062. https://doi.org/10.1098/rspb.2012.3062
Kobayashi T, Okamoto K, Hori Y (2001) Variations in size structure, growth and reproduction in Japanese plantain (Plantago asiatica L.) between exposed and shaded populations. Plant Species Biol 16:13–28. https://doi.org/10.1046/j.1442-1984.2001.00053.x
Kong CH, Zhang SZ, Li YH, Xia ZC, Yang XF, Meiners SJ, Wang P (2018) Plant neighbour detection and allelochemical response are driven by root-secreted signalling chemicals. Nat Commun 9:3867. https://doi.org/10.1038/s41467-018-06429-1
Korb J, Foster KR (2010) Ecological competition favours cooperation in termite societies. Ecol Lett 13:754–760. https://doi.org/10.1111/j.1461-0248.2010.01471.x
Kristensen L, Olsen J, Weiner J (2008) Crop density, sowing pattern, and nitrogen fertilization effects on weed suppression and yield in spring wheat. Weed Sci 56:97–102. https://doi.org/10.1614/WS-07-065.1
Kuiper PJC, Bos M (1992) Plantago: A multidisciplinary study. Springer, Berlin
Lambert D (1992) Zero-inflated poisson regression, with an application to defects in manufacturing. Technometrics 34:1–14. https://www.jstor.org/stable/1269547
Lehmann L, Feldman MW, Rousset F (2009) On the evolution of harming and recognition in finite panmictic and infinite structured populations. Evolution 63:2896–2913. https://doi.org/10.1111/j.1558-5646.2009.00778.x
Murphy GP, Dudley SA (2009) Kin recognition: competition and cooperation in Impatiens (Balsaminaceae). Am J Bot 96:1990–1996. https://doi.org/10.3732/ajb.0900006
Novoplansky A (2009) Picking battles wisely: plant behaviour under competition. Plant Cell Environ 32:726–741. https://doi.org/10.1111/j.1365-3040.2009.01979.x
Pierik R, Mommer L, Voesenek LACJ (2012) Molecular mechanisms of plant competition: neighbour detection and response strategies. Funct Ecol 27:841–853. https://doi.org/10.1111/1365-2435.12010
R Development Core Team (2015) R A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Semchenko M, Hutchings MJ, John EA (2007) Challenging the tragedy of the commons in root competition: confounding effects of neighbour presence and substrate volume. J Ecol 95:252–260. https://doi.org/10.1111/j.1365-2745.2007.01210.x
Semchenko M, Saar S, Lepik A (2014) Plant root exudates mediate neighbour recognition and trigger complex behavioural changes. New Phytol 204:631–637. https://doi.org/10.1111/nph.12930
Takigahira H, Yamawo A (2019) Competitive responses based on kin-discrimination underlie variations in leaf functional traits in Japanese beech (Fagus crenata) seedlings. Evol Ecol 33:521–531. https://doi.org/10.1007/s10682-019-09990-3
Tanaka S, Miura R, Tominaga T (2010) Small-scale heterogeneity in the soil environment influences the distribution of lawn grass and weeds. Weed Biol Manag 10:209–218. https://doi.org/10.1111/j.1445-6664.2010.00386.x
Turkington R, Harper JL (1979) The growth, distribution and neighbour relationships of Trifolium repens in a permanent pasture. I. Ordination, pattern and contact. J Ecol 67:201–218. https://doi.org/10.2307/2259345
Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935. https://doi.org/10.1046/j.1365-294X.2004.02076.x
Weiner J, Griepentrog HW, Kristensen L (2001) Suppression of weeds by spring wheat Triticum aestivum increases with crop density and spatial uniformity. J Appl Ecol 38:784–790. https://doi.org/10.1046/j.1365-2664.2001.00634.x
West SA, Griffin AS, Gardner A (2007) Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol 20:415–432. https://doi.org/10.1111/j.1420-9101.2006.01258.x
Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES IV (2002) Genetic diversity and selection in the maize starch pathway. Proc Natl Acad Sci USA 20:12959–12962. https://doi.org/10.1073/pnas.202476999
Wilson JN (1988) A review of evidence on the control of shoot: root ratio, in relation to models. Ann Bot 61:433–449. https://doi.org/10.1093/oxfordjournals.aob.a087575
Yamawo A (2015) Relatedness of neighboring plants alters the expression of indirect defense traits in an extrafloral nectary-bearing plant. Evol Biol 42:12–19. https://doi.org/10.1007/s11692-014-9295-2
Yamawo A, Mukai H (2017) Seeds integrate biological information about conspecific and allospecific neighbours. Proc R Soc B 284:1857. https://doi.org/10.1098/rspb.2017.0800
Yamawo A, Sato M, Mukai H (2017) Experimental evidence for benefit of self discrimination in roots of a clonal plant. AoB PLANTS 9:plx049. https://doi.org/10.1093/aobpla/plx049
Acknowledgements
We thank Drs J.C. Cahill, and R. Iritani for many useful comments on the manuscript. Work was supported in part by Research Fellowships from the Japan Society for the Promotion of Science (JSPS) for Young Scientists (234305) to A. Y.. This work was also supported by JSPS Grant-in-Aid for Young Scientists (B) (grant no. 18K19353 and 19H03295 to A.Y., grant no. 15K18618 to H. M.).
Author information
Authors and Affiliations
Contributions
A.Y. and H.M. developed the core idea and designed the experiments. A.Y. carried out all experiments and performed data analyses. A.Y. and H.M. wrote the article.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Communicated by Casey p terHorst.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yamawo, A., Mukai, H. Outcome of interspecific competition depends on genotype of conspecific neighbours. Oecologia 193, 415–423 (2020). https://doi.org/10.1007/s00442-020-04694-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04694-w