Previous studies demonstrated the effects of polyploidy on various aspects of plant life. It is, however, difficult to determine which plant characteristics are responsible for fitness differences between cytotypes. We assessed the relationship between polyploidy and seed production. To separate the effects of flowering phenology, flower head size and herbivores from other possible causes, we collected data on these characteristics in single flower heads of diploid and tetraploid Centaurea phrygia in an experimental garden. We used structural equation modelling to identify the main pathways determining seed production. The results showed that the relationship between polyploidy and seed production is mediated by most of the studied factors. The different factors acted in opposing directions. Wider flower heads displayed higher above the ground suggested higher seed production in diploids. In contrast, earlier flowering and a lower abundance of herbivores suggested higher seed production in tetraploids. However, because phenology was the strongest driver of seed production in this system, the sum of all the pathways suggested greater seed production in tetraploids than in diploids. The pathway linking ploidy level directly to seed production, representing unstudied factors, was not significant. This suggests that the factors studied likely are drivers of the between-cytotype differences. Overall, this study demonstrated that tetraploids possess overall higher fitness estimated as seed production. Regardless of the patterns observed here, strong between year fluctuations in the composition and diversity of insect communities have been observed. The direction of the selection may thus vary between years. Consequently, understanding the structure of the interactions is more important for understanding the system than the overall effects of cytotype on a fitness trait in a specific year. Such knowledge can be used to model the evolution of species traits and plant-herbivore and plant-pollinator interactions in diploid-polyploid systems.

Department of Botany Faculty of Science Charles University Prague Czech Republic

Group Function of Invertebrate and Plant Biodiversity in Agro ecosystems Crop Research Institute Prague Czech Republic

Institute of Botany Academy of Sciences of the Czech Republic Průhonice Czech Republic

Zobrazit více v PubMed

Arvanitis L, Wiklund C, Münzbergová Z, Dahlgren JP, Ehrlén J. 2010. Novel antagonistic interactions associated with plant polyploidization influence trait selection and habitat preference. Ecology Letters 13:330–337. PubMed

Boalt E, Arvanitis L, Lehtila K, Ehrlén J. 2010. The association among herbivory tolerance, ploidy level, and herbivory pressure in

Bolmgren K, Eriksson O. 2015. Are mismatches the norm? Timing of flowering, fruiting, dispersal and germination and their fitness effects in

Borges LA, Souza LGR, Guerra M, Machado IC, Lewis GP, Lopes AV. 2012. Reproductive isolation between diploid and tetraploid cytotypes of

Buggs RJA, Pannell JR. 2007. Ecological differentiation and diploid superiority across a moving ploidy contact zone. Evolution 61:125–140. PubMed

Burt MA, Dunn RR, Nichols LM, Sanders NJ. 2014. Interactions in a warmer world: effects of experimental warming, conspecific density, and herbivory on seedling dynamics. Ecosphere 5:9

Burton TL, Husband BC. 2000. Fitness differences among diploids, tetraploids, and their triploid progeny in PubMed

Burton TL, Husband BC. 2001. Fecundity and offspring ploidy in matings among diploid, triploid and tetraploid PubMed

Campbell DR, Powers JM. 2015. Natural selection on floral morphology can be influenced by climate. Proceedings of the Royal Society B-Biological Sciences 282:7. PubMed PMC

Caruso I, Lepore L, De Tommasi N, Dal Piaz F, Frusciante L, Aversano R, Garramone R, Carputo D. 2011. Secondary metabolite profile in induced tetraploids of wild PubMed

Castro S, Münzbergová Z, Raabová J, Loureiro J. 2011. Breeding barriers at a diploid–hexaploid contact zone in

Černá L, Münzbergová Z. 2013. Comparative population dynamics of two closely related species differing in ploidy level. PLoS One 8: e75563. PubMed PMC

Černá L, Münzbergová Z. 2015. Conditions in home and transplant soils have differential effects on the performance of diploid and allotetraploid PubMed PMC

Červenková Z, Münzbergová Z. 2014. Pollen limitation and pollinator preferences in PubMed

Cohen H, Fait A, Tel-Zur N. 2013. Morphological, cytological and metabolic consequences of autopolyploidization in PubMed PMC

Comai L. 2005. The advantages and disadvantages of being polyploid. Nature Reviews Genetics 6:836–846. PubMed

De Jesus-Gonzalez L, Weathers PJ. 2003. Tetraploid PubMed

Dostálek T, Münzbergová Z. 2013. Comparative population biology of critically endangered

Ehrlén J, Münzbergová Z. 2009. Timing of flowering: opposed selection on different fitness components and trait covariation. American Naturalist 173:819–830. PubMed

Ehrlén J, Raabová J, Dahlgren JP. 2015. Flowering schedule in a perennial plant; life-history trade-offs, seed predation, and total offspring fitness. Ecology 96:2280–2288. PubMed

Eliášová A, Trávníček P, Mandák B, Münzbergová Z. 2014. Autotetraploids of PubMed PMC

Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G. 2007. Time after time: flowering phenology and biotic interactions. Trends in Ecology & Evolution 22:432–439. PubMed

Gomez JM. 2003. Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb PubMed

Grace J, Bollen K. 2005. Interpreting the results from multiple regression and structural equation models. Bulletin of the Ecological Society of America 86:283–294.

Grace JB. 2003. Comparing groups using structural equations In: Pugesek B, Tomer A, von Eye A, eds. Structural equation modeling. Applications in ecological and evolutionary biology. Cambridge: Cambridge University Press.

Grindeland JM, Sletvold N, Ims RA. 2005. Effects of floral display size and plant density on pollinator visitation rate in a natural population of

Gross K, Schiestl FP. 2015. Are tetraploids more successful? Floral signals, reproductive success and floral isolation in mixed-ploidy populations of a terrestrial orchid. Annals of Botany 115:263–273. PubMed PMC

Hafdahl CE, Craig TP. 2014. Flowering phenology in

Halverson K, Heard SB, Nason JD, Stireman JO. 2008. Differential attack on diploid, tetraploid, and hexaploid PubMed

Hulber K, Haider JA, Hager TE, Dullinger S, Fiedler K. 2015. Insect herbivory in alpine grasslands is constrained by community and host traits. Journal of Vegetation Science 26:663–673.

Husband BC, Ozimec B, Martin SL, Pollock L. 2008. Mating consequences of polyploid evolution in flowering plants: current trends and insights from synthetic polyploids. International Journal of Plant Sciences 169:195–206.

Husband BC, Sabara HA. 2004. Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, PubMed

Husband BC, Schemske DW. 2000. Ecological mechanisms of reproductive isolation between diploid and tetraploid

Jersáková J, Castro S, Sonk N, Milchreit K, Schodelbauerová I, Tolasch T, Dotterl S. 2010. Absence of pollinator-mediated premating barriers in mixed-ploidy populations of

Jordan CY, Ally D, Hodgins KA. 2015. When can stress facilitate divergence by altering time to flowering? Ecology and Evolution 5:S962–S973. PubMed PMC

Kameyama Y, Kudo G. 2015. Intrinsic and extrinsic factors acting on the reproductive process in alpine-snowbed plants: roles of phenology, biological interaction, and breeding system. Plant Species Biology 30:3–15.

Karron JD, Mitchell RJ. 2012. Effects of floral display size on male and female reproductive success in PubMed PMC

Kim TN, Underwood N. 2015. Plant neighborhood effects on herbivory: damage is both density and frequency dependent. Ecology 96:1431–1437. PubMed

Koch K. 1992. Die käfer mitteleuropas. Ökologie: Goecke and Evers, Krefeld.

Konig MAE, Wiklund C, Ehrlén J. 2015. Timing of flowering and intensity of attack by a butterfly herbivore in a polyploid herb. Ecology and Evolution 5:1863–1872. PubMed PMC

Koprdova S, Bellanger S, Skuhrovec J, Darmency H. 2015. Does gall midge larvae cause pre-dispersal seed mortality and limit cornflower population growth? Acta Oecologica-International Journal of Ecology 69:167–172.

Koutecký P, Štěpánek J, Bad'urová T. 2012. Differentiation between diploid and tetraploid

Lavania UC, Srivastava S, Lavania S, Basu S, Misra NK, Mukai Y. 2012. Autopolyploidy differentially influences body size in plants, but facilitates enhanced accumulation of secondary metabolites, causing increased cytosine methylation. Plant Journal 71:539–549. PubMed

Lee SY. 2007. Structural equation modeling: a Bayesian approach. United Kingdom: John Wiley and Sons.

Lehndal L, Agren J. 2015. Herbivory differentially affects plant fitness in three populations of the perennial herb PubMed PMC

Lepš J, Šmilauer P. 2003. Multivariate analysis ecological data using CANOCO. Cambridge: Cambridge University Press.

Leschen R, Beutel R, Lawrence J. 2010. Handbook of zoology, coleoptera volume 2: morphology and systematics (elateroidea, bostrichformia, cucujiformia partim). Berlin: Walter de Gruyter.

Lobo JA, Ramos DD, Braga AC. 2016. Visitation rate of pollinators and nectar robbers to the flowers and inflorescences of

Loranger J, Meyer ST, Shipley B, Kattge J, Loranger H, Roscher C, Weisser WW. 2012. Predicting invertebrate herbivory from plant traits: evidence from 51 grassland species in experimental monocultures. Ecology 93:2674–2682. PubMed

Lumaret R. 1988. Adaptive strategies and ploidy levels. Acta Oecologica-Oecologia Plantarum 9:83–93.

Maherali H, Walden AE, Husband BC. 2009. Genome duplication and the evolution of physiological responses to water stress. New Phytologist 184:721–731. PubMed

Martínková Z, Honěk A. 2008. Contrast adaptation to time constraints on development of two pre-dispersal predators of dandelion (

Merz B. 1994. Diptera: Tephritidae Insecta helvetica fauna. Geneva, Switzerland: Hge. Press.

Munguia-Rosas MA, Ollerton J, Parra-Tabla V, De-Nova JA. 2011. Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecology Letters 14:511–521. PubMed

Münzbergová Z. 2007. Population dynamics of diploid and hexaploid populations of a perennial herb. Annals of Botany 100:1259–1270. PubMed PMC

Münzbergová Z. 2005. Determinants of species rarity: population growth rates of species sharing the same habitat. American Journal of Botany 92:1987–1994. PubMed

Münzbergová Z. 2006a. Ploidy level interacts with population size and habitat conditions to determine the degree of herbivory damage in plant populations. Oikos 115:443–452.

Münzbergová Z. 2006b. Effect of population size on the prospect of species survival. Folia Geobotanica 41:137–150.

Münzbergová Z, Skuhrovec J. 2013. Effect of habitat conditions and plant traits on leaf damage in the Carduoideae subfamily. PLoS One 8:9. PubMed PMC

Münzbergová Z, Skuhrovec J, Maršík P. 2015. Large differences in the composition of herbivore communities and seed damage in diploid and autotetraploid plant species. Biological Journal of the Linnean Society 115:270–287.

Nartshuk E. 2010. Grassflies of the genus Polyodaspis Duda (Diptera, Chloropidae) in the fauna of Southeast Asia. Entomological Review 90:946–950.

Nuismer SL, Cunningham BM. 2005. Selection for phenotypic divergence between diploid and autotetraploid PubMed

Nuismer SL, Ridenhour BJ. 2008. The contribution of parasitism to selection on floral traits in PubMed

Nuismer SL, Thompson JN. 2001. Plant polyploidy and non-uniform effects on insect herbivores. Proceedings of the Royal Society B-Biological Sciences 268:1937–1940. PubMed PMC

Oswald BP, Nuismer SL. 2011. Neopolyploidy and diversification in PubMed PMC

Otto SP. 2007. The evolutionary consequences of polyploidy. Cell 131:452–462. PubMed

Otto SP, Whitton J. 2000. Polyploid incidence and evolution. Annual Review of Genetics 34:401–437. PubMed

Perez-Barrales R, Bolstad GH, Pelabon C, Hansen TF, Armbruster WS. 2013. Pollinators and seed predators generate conflicting selection on

Petit C, Bretagnolle F, Felber F. 1999. Evolutionary consequences of diploid–polyploid hybrid zones in wild species. Trends in Ecology & Evolution 14:306–311. PubMed

Petit C, Lesbros P, Ge XJ, Thompson JD. 1997. Variation in flowering phenology and selfing rate across a contact zone between diploid and tetraploid

Pugesek B, Tomer A, von Eye A. 2003. Structural equation modeling. Applications in ecological and evolutionary biology

R Development Core Team. 2011. A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Ramsey J, Ramsey TS. 2014. Ecological studies of polyploidy in the 100 years following its discovery. Philosophical Transactions of the Royal Society B-Biological Sciences 369:20. PubMed PMC

Ramsey J, Schemske DW. 2002. Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33:589–639.

Repcak M, Krausová T. 2009. Phenolic glucosides in the course of ligulate flower development in diploid and tetraploid

Rieder JP, Evans EW, Durham SL. 2001. Distribution of insect attacks in biological control of weeds: infestation of

Scheiner S, Callahan H. 1999. Measuring natural selection on phenotypic plasticity. Evolution 53:1704–1713. PubMed

Scheiner SM, Mitchell RJ, Callahan HS. 2000. Using path analysis to measure natural selection. Journal of Evolutionary Biology 13:423–433.

Schlinkert H, Westphal C, Clough Y, Laszlo Z, Ludwig M, Tscharntke T. 2015. Plant size as determinant of species richness of herbivores, natural enemies and pollinators across 21 Brassicaceae species. PLoS One 10: 0135928 PubMed PMC

Schoonhoven L, van Loon J, Dicke M. 1998. Insect-plant biology. London: Chapman and Hall.

Segraves KA, Anneberg TJ. 2016. Species interactions and plant polyploidy. American Journal of Botany 103: 1326–1335. PubMed

Segraves KA, Thompson JN. 1999. Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid PubMed

Skuhravá M. 1994. The zoogeography of gall midges (Cecidomyiidae, Diptera) of the Czech Republic. II. Review of gall midge species including zoogeographical diagnoses. Acta Societatis Zoologicae Bohemoslovenicae 58:41–88.

Skuhrovec J, Koprdová S, Mikulka J. 2008. How can seed feeders regulate dispersion of thistles,

Sletvold N, Moritz KK, Agren J. 2015. Additive effects of pollinators and herbivores result in both conflicting and reinforcing selection on floral traits. Ecology 96:214–221. PubMed

Smith DS, Lamit LJ, Lau MK, Gehring CA, Shuster SM, Whitham TG. 2015. Introduced elk alter traits of a native plant and its plant-associated arthropod community. Acta Oecologica-International Journal of Ecology 67:8–16.

Sober V, Teder T, Moora M. 2009. Contrasting effects of plant population size on florivory and pollination. Basic and Applied Ecology 10:737–744.

ter Braak C, Šmilauer P. 1998. Canoco reference manual and users guide to canoco for windows: software for canonical community ordination (version 4). Ithaca: Microcomputer Power.

Thompson JN, Cunningham BM, Segraves KA, Althoff DM, Wagner D. 1997. Plant polyploidy and insect/plant interactions. American Naturalist 150:730–743. PubMed

Thompson JN, Nuismer SL, Merg K. 2004. Plant polyploidy and the evolutionary ecology of plant/animal interactions. Biological Journal of the Linnean Society 82:511–519.

Trudgill DL, Honěk A, Li D, Van Straalen NM. 2005. Thermal time—concepts and utility. Annals of Applied Biology 146:1–14.

Van Dijk P, Bijlsma R. 1994. Simulations of flowering time displacement between 2 cytotypes that form inviable hybrids. Heredity 72:522–535.

Van Dijk P, Van Delden W. 1990. Evidence for autotetraploidy in

Vanhoenacker D, Agren J, Ehrlén J. 2013. Non-linear relationship between intensity of plant-animal interactions and selection strength. Ecology Letters 16:198–205. PubMed

Varga S. 2014. Pre-dispersal seed predation in gynodioecious

Volovnik SV. 2016. On oviposition in weevils of the genus

Weber A, Kolb A. 2013. Local plant density, pollination and trait-fitness relationships in a perennial herb. Plant Biology 15:335–343. PubMed

Zwölfer H, Frick K, Andres L. 1971. A study of the host plant relationships of European members of the genus

Data on Herbivore Performance and Plant Herbivore Damage Identify the Same Plant Traits as the Key Drivers of Plant-Herbivore Interaction