Abstract
Presence of a root neighbor can induce changes in root allocation and pollen traits, but only a limited number of studies have investigated such effects on pollen. To learn more about effects of root contact on pollen competitive ability, we studied plants of the hermaphroditic winter-annual Collinsia heterophylla, native to California. We cultivated plants in two-pot treatments with roots kept either separate or intermingled with the same amount of resources. Pollen-tube growth rate, as an indication of pollen competitive ability, was affected by root treatment but the response varied among competing plant families. The response to root-treatment was not an effect of differential resource uptake of the two competitors. Root biomass was significantly higher when roots were intermingled compared to separate. This finding adds to the number of species with a strategic root response in the presence of competitors, but could also be a consequence of a larger rooting volume. Allocation to pollen performance versus roots in the presence of a competitor was lower in small plants and higher in large plants, potentially implying high costs of producing competitive pollen. We conclude that our study demonstrated that pollen tube growth rate is highly sensitive to the root environment in C. heterophylla.
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References
Aarssen LW (2000) Why are most selfers annuals? A new hypothesis for the fitness benefit of selfing. Oikos 3:606–612
Armbruster WS, Mulder CPH, Baldwin BG, Kalisz S, Wessa B, Nute H (2002) Comparative analysis of late floral development and mating-system evolution in tribe Collinsieae (Scrophulariaceae s.l.). Am J Bot 89:37–49
Arnold SJ (1994) Bateman's principles and the measurement of sexual selection in plants and animals. Am Nat suppl 144:S126–S128
Ashman T-L (2006) The evolution of seprarate sexes: a focus on the ecological context. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford Univ Press, New York, pp 204–222
Ashman T-L, Baker I (1992) Variation in floral sex allocation with time of season and currency. Ecology 73:1237–1243
Belter PR, Cahill JF (2015) Disentangling root system responses to neighbours: identification of novel root behavioural strategies. AoB Plants 7:plv059
Bernasconi G, Ashman T-L, Birkhead TR, Bishop JDD, Grossniklaus U, Kubli E, Marshall DL, Schmid B, Skogsmyr I, Snook RR, Taylor D, Till-Bottraud I, Ward PI, Zeh DW, Hellriegel B (2004) Evolutionary ecology of the prezygotic stage. Science 303:971–975
Bertin RI (1988) Paternity in plants. In: Lovett Doust J, Lovett Doust L (eds) Plant reproductive ecology: patterns and strategies. Oxford Univ Press, New York, pp 30–59
Cahill JF, McNickle GG (2011) The behavioural ecology of nutrient foraging by plants. Annu Rev Ecol Evol Syst 42:289–311
Cahill JF, McNickle GG, Haag JJ, Lamb EG, Nyanumba SM, St Clair CC (2010) Plants integrate information about nutrients and neighbors. Science 328:1657
Callaway RM (2002) The detection of neighbors by plants. Trends Ecol Evol 17:104–105
Campbell DR (2000) Experimental tests of sex-allocation theory in plants. Trends Ecol Evol 15:227–232
Cao G-X, Kudo G (2008) Size-dependent sex allocation in a monocarpic perennial herb, Cardiocrinum cordatum (Liliaceae). Plant Ecol 194:99–107
Charnov EL (1980) Sex allocation and local mate competition in barnacles. Mar Biol Lett 1:269–272
Charnov EL (1982) The theory of sex allocation. Princeton Univ Press, Princeton
Chen BJW, During HJ, Anten NPR (2012) Detect thy neighbor: identity recognition at the root level in plants. Plant Sci 195:157–167
Chen BJW, During HJ, Vermeulen PJ, de Kroon H, Poorter H, Anten NPR (2015) Corrections for rooting volume and plant size reveal negative effects of neighbor presence on root allocation in pea. Funct Ecol. doi:10.1111/1365-2435.12450
Cocucci AA, Marino S, Baranzelli M, Wiemer AP, Sersic A (2014) The buck in the milkweed: evidence of male-male interference among pollinaria on pollinators. New Phytol 203:280–286
de Jong T, Klinkhamer P (2005) Evolutionary ecology of plant reproductive strategies. Cambridge Univ Press, Cambridge
Delph LF, Ashman T-L (2006) Trait selection in fl owering plants: how does sexual selection contribute? Integr Comp Biol 46:465–472
Delph LF, Johansson MH, Stephenson AG (1997) How environmental factors affect pollen performance: ecological and evolutionary perspectives. Ecology 78:1632–1639
Depuydt S (2014) Arguments for and against self and non-self root recognition in plants. Front Plant Sci 5:614
Dudley SA, Murphy GP, File AL (2013) Kin recognition and competition in plants. Funct Ecol 27:898–906
Falster DS, Westoby M (2003) Plant height and evolutionary games. Trends Ecol Evol 18:337–343
Fang S, Clark RT, Zheng Y, Iyer-Pacuzzi AS, Weitz JS, Kochian LV, Edelsbrunner H, Liao H, Benfey PN (2013) Genotypic recognition and spatial responses by rice roots. PNAS 110:2670–2675
Gersani M, Brown JS, O’Brien EE, Mania GM, Abramsky Z (2001) Tradegy of the commons as a result of root competition. J Evol 89:660–669
Harder LC, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature 373:512–515
Harris MS, Pannell JR (2008) Roots, shoots and reproduction: sexual dimorphism in size and costs of reproductive allocation in an annual herb. Proc R Soc B 275:2595–2602
Hess L, de Kroon H (2007) Effects of rooting volume and nutrient availability as an alternative explaination for root self/non-self discrimination. J Ecol 95:241–251
Hoekstra FA, Bruinsma J (1975) Respiration and vitality of binucleate and trinucleate pollen. Physiol Plant 34:221–225
Ishida TA, Hattori K, Shibata S, Suzuki M, Kimura MT (2005) Sex allocation of a cosexual wind-pollinated tree, Quercus dentata, in terms of four currencies. J Plant Res 118:193–197
Jannike T, Marie-Orleach L, De Mulder K, Berezikov E, Ladurner P, Vizoso DB, Schärer L (2013) Sex allocation adjustment to mating group size in a simultaneous hermaphrodite. Evolution 67:3233–3242
Klinkhamer PGL, de Jong TJ (1997) Size-dependent allocation to male and female reproduction. In: Bazzaz EA, Grace J (eds) Plant resource allocation. Academic Press, San Diego, pp 221–229
Klinkhamer PGL, de Jong TJ, Bruyn GJ (1989) Plant size and pollinator visitation in Cynoglossum officinale. Oikos 54:201–204
Klinkhamer PGL, de Jong TJ, Metz H (1997) Sex and size in cosexual plants. Trends Ecol Evol 12:260–265
Lankinen Å (2000) Effects of soil pH and phosphorus on in vitro pollen competitive ability and sporophytic traits in clones of Viola tricolor. Int J Plant Sci 161:885–893
Lankinen Å (2008) Root competition influences pollen competitive ability in Viola tricolor: effects of presence of a competitor beyond resource availability. J Ecol 96:756–765
Lankinen Å, Armbruster WS (2007) Pollen competition reduces inbreeding depression in Collinsia heterophylla (Plantaginaceae). J Evol Biol 20:737–749
Lankinen Å, Green KK (2015) Using theories of sexual selection and sexual conflict to improve our understanding of plant ecology and evolution. AoB Plants 7:plv008
Lankinen Å, Madjidian JA (2011) Enhancing pollen competition by delaying stigma receptivity: pollen deposition schedules affect siring ability, paternal diversity, and seed production in Collinsia heterophylla (Plantaginaceae). Am J Bot 98:1191–1200
Lankinen Å, Armbruster WS, Antonsen L (2007) Delayed stigma receptivity in Collinsia heterophylla (Plantaginaceae): genetic variation and adaptive significance in relation to pollen competition, delayed self-pollination, and mating system evolution. Am J Bot 94:1183–1192
Lankinen Å, Maad J, Armbruster WC (2009) Pollen-tube growth rates in Collinsia heterophylla (Plantaginaceae): one-donor crosses reveal heritability but no effect on sporophytic-offspring fitness. Ann Bot 103:941–950
Lankinen Å, Larsson MC, Fransson AM (2013) Allocation to pollen competitive ability versus seed production in Viola tricolor as an effect of plant size, soil nutrients and presence of a root competitor. Oikos 122:779–789
Lankinen Å, Smith HG, Andersson S, Madjidian JA (2016) Selection on pollen and pistil traits during pollen competition is affected by both sexual conflict and mixed mating in a self-compatible herb. Am J Bot (in press)
Lau TC, Stephenson AG (1993) Effects of soil nitrogen on pollen production, pollen grain size and pollen performance in Cucurbita pepo. Am J Bot 80:763–768
Lloyd DG, Bawa KS (1984) Modification of the gender of seed plants in varying conditions. Evol Biol 17:255–388
Madjidian JA, Lankinen Å (2009) Sexual conflict and sexually antagonistic coevolution in an annual plant. PLoS ONE 4:e5477
Maina GG, Brown JS, Gersani M (2002) Intra-plant versus interplant root competition in beans: avoidance, resource matching or tragedy of the commons. Plant Ecol 160:235–247
Markham J, Halwas S (2011) Effect of neighbour presence and soil volume on the growth of Andrpogon gerardii Vitman. Plant Ecol Divers 4:265–268
McNickle GG, Brown JS (2014) An ideal free distribution explains the root production of plants that do not engage in a tragedy of the commons game. J Ecol 102:963–971
Meier IC, Angert A, Falik O, Shelef O, Rachmilevitch S (2013) Increased root oxygen uptake in pea plants responding to non-self neighbors. Planta 238:577–586
Mossberg B (1992) Den nordiska floran. Wahlström och Widstrand, Stockholm
Neese EC (1993) Collinsia. In: Hickman JC (ed) The Jepson manual: higher plants of California. Univ of California Press, Berkeley, pp 1024–1027
Newsom VM (1929) A revision of the genus Collinsia. Bot Gaz 87:260–301
Nord EA, Zhang C, Lynch JP (2011) Root responses to neighbouring plants in common beans are mediated by nutrient concentration rather than self/non-self recognition. Funct Plant Biol 38:941–952
Novopolansky A (2009) Picking battles wisely: plant behaviour under competition. Plant Cell Environ 32:726–741
O’Brien EE, Brown JS (2008) Games roots play: effects of soil volume and nutrients. J Ecol 96:438–446
O’Brien EE, Gersani M, Brown JS (2005) Root proliferation and seed yield in response to spatial heterogeneity of below-ground competition. New Phytol 168:401–412
Pannell J (1997) Variation in sex ratios and sex allocation in androdioecious Mercuralis annua. J Ecol 85:57–69
Pasonen HL, Pulkkinen P, Käpylä M, Blom A (1999) Pollen tube growth rate and seed siring success among Betula pendula clones. New Phytol 143:243–251
Pierik R, Mommer L, Voesenek LACJ (2013) Molecular mechanisms of plant competition: neighbor detection and response strategies. Funct Ecol 27:841–853
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50
Queller DC (1984) Models of kin selection on seed provisioning. Heredity 53:151–165
Schärer L (2009) Test of sex allocation theory in simultaneously hermaphroditic animals. Evolution 63:1377–1405
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
Semchenko M, Saar S, Lepik A (2014) Plant root exudates mediate neighbor recognition and trigger complex behavioural changes. New Phytol 204:631–637
Skogsmyr I, Lankinen Å (1999) Selection on pollen competitive ability in relation to stochastic factors influencing pollen deposition. Evol Ecol Res 1:971–985
Snow AA, Spira TP (1991) Pollen vigour and the potential for sexual selection in plants. Nature 352:796–797
Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. WH Freeman & Co, New York
SPSS 20.0 (2014) SPSS. Syntax Reference Group, SPSS Inc, Chicago
Stephenson AG, Travers SE, Mena-Ali JI, Winsor JA (2003) Pollen performance before and during the autotrophic-heterotrophic transition of pollen tube growth. Philos Trans R Soc Lond B Biol Sci 358:1009–1018
Tosti G, Thorup-Kristensen K (2010) Using coloured roots to study root interaction and competition in intercropped legumes and non-legumes. J Plant Ecol 3:191–199
Vega-Fruits R, Macías-Ordóñez R, Guevara R, Fromhage L (2014) Sex change in plants and animals: a unified perspective. J Evol Biol 27:667–675
Vilas JS, Pannell JR (2012) Do plants adjust their sex allocation and secondary sexual morphology in response to their neighbours? Ann Bot 110:1471–1478
Wang P, Weiner J, Cahill JF, Zhou DW, Bian HF, Song YT, Sheng LX (2014) Shoot competition, root competition and reproductive allocation in Chenopodium acuminatum. J Ecol 102:1688–1696
Weiner J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol Evol Syst 6:207–215
Willi Y (2013) The battle of the sexes over seed size: support for both kinship genomic imprinting and interlocus contest evolution. Am Nat 181:787–798
Willson MF, Burley N (1983) Mate choice in plants: tactics, mechanisms and consequences. Princeton Univ Press, Princeton
Acknowledgments
We thank L-M Mårtensson for comments on the text. Financial support was provided by the Swedish Research Council (to Å.L.).
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Lankinen, Å., Niss, J. & Madjidian, J.A. Effect of root contact on pollen competitive ability in a hermaphroditic winter-annual herb. Evol Ecol 30, 739–754 (2016). https://doi.org/10.1007/s10682-016-9839-2
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DOI: https://doi.org/10.1007/s10682-016-9839-2