Local loss of the zebra-like coloration supports the aposematic and other visual defense hypotheses in Silybum marianum

In: Israel Journal of Plant Sciences

ABSTRACT

The question of the spread of an aposematic or of an otherwise visually defended plant type within a non-aposematic or a visually non-defended population is a long-standing enigma that has received considerable theoretical attention. However, the spreading of aposematic or otherwise visually defended plant genotypes within a non-aposematic or a non-visually-defended population has never, as far as is known, been shown or studied in nature in wild plant populations. This study investigates the loss of the various simultaneous types of defensive coloration in the spiny thistle Silybum marianum by a mutation that occurred independently and found in 13 wild populations in Israel. Mutant plants have plain leaves rather than leaves of the zebra-like wild-type, which has a white network of stripes on the upper leaf surface. The mutants never spread beyond several dozen meters and usually only over several meters. The mutation has a simple developmental origin, since the white variegation is the result of small air spaces formed between the epidermis and the photosynthetic parenchyma (causing no loss of photosynthetic capacity in white areas), and the mutants have no such subepidermal air spaces. In order to examine the possibility of establishing a pure population lacking this type of defensive coloration, seeds of mutant plants were collected from two wild populations where they grew mixed with the wild-type and a pure mutant population was selected and maintained for 4 years. Thus, 13 cases of very restricted spread of the visually defenseless mutant demonstrate the probable contribution of the variegation to plant fitness, supporting the hypothesis that conspicuous leaf variegation functions as defensive coloration.

  • AllenJA, CooperJM. 1985. Crypsis and masquerade. J Biol Educ. 19:268–270.

  • BatesHW. 1862. Contributions to an insect fauna of the Amazon valley. Lepidoptera: Heliconidae. Trans Linn Soc London. 23:495–566.

  • BradyJ, ShereniW. 1988. Landing responses of the tsetse fly Glossina morsitans morsitans Westwood and the stable fly Stomoxys calcitrans (L.) (Diptera: Glossinidae & Muscidae) to black-and-white patterns: a laboratory study. Bull Entomol Res. 78:301–311.

    • Search Google Scholar
    • Export Citation
  • CottHB. 1940. Adaptive coloration in animals. London: Methuen & Co.

  • DaninA, Yom-TovY. 1990. Ant nests as primary habitats of Silybum marianum (Compositae). Pl Syst Evol. 169:209–217.

  • DokuC, BradyJ. 1989. Landing site preferences of Glossina morsitans morsitans Westwood (Diptera: Glossinidae) in the laboratory: avoidance of horizontal features? Bull Entomol Res. 79:521–528.

    • Search Google Scholar
    • Export Citation
  • EdmundsM. 1974. Defence in animals: a survey of anti-predator defences. Harlow: Longman Group.

  • EgriÁ, BlahóM, KriskaG, FarkasR, GyurkovszkyM, ÅkessonS, HorváthG. 2012. Polarotactic tabanids find striped patterns with brightness and/or polarization modulation least attractive: an advantage of zebra stripes. J Exp Biol. 215:736–745.

    • Search Google Scholar
    • Export Citation
  • EndlerJA. 1981. An overview of the relationships between mimicry and crypsis. Biol J Linn Soc. 16:25–31.

  • Feinbrun-DothanN. 1978. Flora Palaestina. Vol. III. Jerusalem: The Israel Academy of Sciences and Humanities.

  • ForbesP. 2009. Dazzled and deceived: mimicry and camouflage. New Haven, CT: Yale University Press.

  • GabayR, PlitmannU, DaninA. 1994. Factors affecting the dominance of Silybum marianum L. (Asteraceae) in its specific habitats. Flora. 189:201–206.

    • Search Google Scholar
    • Export Citation
  • GibsonG. 1992. Do tsetse flies ‘see’ zebras? A field study of the visual response of tsetse to striped targets. Physiol Entomol. 17:141–147.

    • Search Google Scholar
    • Export Citation
  • HaraN. 1957. Study of the variegated leaves, with special reference to those caused by air spaces. Jap J Bot. 16:86–101.

  • HetzE, LierschR, SchiederO. 1995. Genetic investigations on Silybum marianum and S. eburneum with respect to leaf colour, outcrossing ratio, and flavonolignan composition. Planta Medica. 61:54–57.

    • Search Google Scholar
    • Export Citation
  • KeasarT, GerchmanY, Lev-YadunS. 2016. A seven-year study of flower-color polymorphism in a Mediterranean annual plant. Basic Appl Ecol. 17:741–750.

    • Search Google Scholar
    • Export Citation
  • KendrickJW, TuckerJ, PeoplesSA. 1955. Nitrate poisoning in cattle due to ingestion of variegated thistle, Silybum marianum. J Am Vet Med Assoc. 126:53–56.

    • Search Google Scholar
    • Export Citation
  • Lev-YadunS. 2001. Aposematic (warning) coloration associated with thorns in higher plants. J Theor Biol. 210:385–388.

  • Lev-YadunS. 2003. Why do some thorny plants resemble green zebras? J Theor Biol. 244:483–489.

  • Lev-YadunS. 2009a. Aposematic (warning) coloration in plants. In: BaluskaF, editor. Plant-environment interactions. From sensory plant biology to active plant behavior. Berlin: Springer-Verlag; p. 167–202.

    • Search Google Scholar
    • Export Citation
  • Lev-YadunS. 2009b. Müllerian and Batesian mimicry rings of white-variegated aposematic spiny and thorny plants: a hypothesis. Isr J Plant Sci. 57:107–116.

    • Search Google Scholar
    • Export Citation
  • Lev-YadunS. 2014a. The proposed anti-herbivory roles of white leaf variegation. Prog Bot. 76:241–269.

  • Lev-YadunS. 2014b. Potential defence from herbivory by ‘dazzle effects’ and ‘trickery coloration’ of leaf variegation. Biol J Linn Soc. 111:692–697.

    • Search Google Scholar
    • Export Citation
  • Lev-YadunS. 2014c. Defensive masquerade by plants. Biol J Linn Soc. 113:1162–1166.

  • Lev-YadunS. 2016. Defensive (anti-herbivory) coloration in land plants. Anti-herbivory plant coloration and morphology. Zug: Springer.

  • Lev-YadunS, Ne'emanG, ShanasU. 2009. A sheep in wolf's clothing: do carrion and dung odours of flowers not only attract pollinators but also deter herbivores? BioEssays. 31:84–88.

    • Search Google Scholar
    • Export Citation
  • MalletJ, GilbertLE. 1995. Why are there so many mimicry rings? Correlations between habitat, behaviour and mimicry in Heliconius butterflies. Biol J Linn Soc. 55:159–180.

    • Search Google Scholar
    • Export Citation
  • MalletJ, JoronM. 1999. Evolution of diversity in warning color and mimicry: polymorphisms, shifting balance, and speciation. Annu Rev Ecol Syst. 30:201–233.

    • Search Google Scholar
    • Export Citation
  • MarplesNM, KellyDJ, ThomasRJ. 2005. The evolution of warning coloration is not paradoxical. Evolution. 59:933–940.

  • MidgleyJJ. 2004. Why are spines of African Acacia species white? Afr J Range For Sci. 21:211–212.

  • MorazzoniP, BombardelliE. 1995. Silybum marianum (Carduus marianus). Fitoterapia. 66:3–42.

  • MüllerF. 1879. Ituna and Thyridia; a remarkable case of mimicry in butterflies. Proc Entomol Soc Lond. 1879:xx–xxix.

  • NiemeläP, TuomiJ. 1987. Does the leaf morphology of some plants mimic caterpillar damage? Oikos. 50:256–257.

  • OhgushiT. 2005. Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Syst. 36:81–105.

  • PoultonEB. 1890. The colours of animals. Their meaning and use. Especially considered in the case of insects. 2nd ed. London: Kegan Paul, Trench, Trübner, & Co.

    • Search Google Scholar
    • Export Citation
  • Precipitation map. 1987. Israel Meteorological Service, Ministry of Transport. Bet Dagan.

  • RonelM, Lev-YadunS. 2012. The spiny, thorny and prickly plants in the flora of Israel. Bot J Linn Soc. 168:344–352.

  • RothschildM, MooreB. 1987. Pyrazines as alerting signals in toxic plants and insects. In: LabeyrieV, FabresG, LachaiseD, editors. Insects – plants. Dordrecht: Dr W. Junk Publishers; p. 97–101.

    • Search Google Scholar
    • Export Citation
  • RubinoDL, McCarthyBC. 2004. Presence of aposematic (warning) coloration in vascular plants of southeastern Ohio. J Torrey Bot Soc. 131:252–256.

    • Search Google Scholar
    • Export Citation
  • RuxtonGD. 2009. Non-visual crypsis: a review of the empirical evidence for camouflage to senses other than vision. Phil Trans R Soc B. 364:549–557.

    • Search Google Scholar
    • Export Citation
  • RuxtonGD, SherrattTN, SpeedMP. 2004. Avoiding attack. The evolutionary ecology of crypsis, warning signals & mimicry. Oxford: Oxford University Press.

    • Search Google Scholar
    • Export Citation
  • ScarchukJ, LentJM. 1965. The structure of mottled-leaf summer squash. J Hered. 56:167–168.

  • SchaeferHM, RuxtonGD. 2011. Plant-animal communication. New York: Oxford University Press.

  • ShmidaA. 1985. Why do some Compositae have an inconsistently deciduous pappus? Ann Missouri Bot Gard. 72:184–186.

  • SkelhornJ. 2015. Masquerade. Curr Biol. 25:R643–R644.

  • SkelhornJ, RowlandHM, DelfJ, SpeedMP, RuxtonGD. 2011. Density-dependent predation influences the evolution and behavior of masqueradinf prey. Proc Natl Acad Sci USA. 108:6532–6536.

    • Search Google Scholar
    • Export Citation
  • SkelhornJ, RowlandHM, RuxtonGD. 2010a. The evolution and ecology of masquerade. Biol J Linn Soc. 99:1–8.

  • SkelhornJ, RowlandHM, SpeedMP, RuxtonGD. 2010b. Masquerade: camouflage without crypsis. Science. 327:51.

  • SkelhornJ, RowlandHM, SpeedMP, De WertL, QuinnL, DelfJ, RuxtonGD. 2010c. Size-dependent misclassification of masquerading prey. Behav Ecol. 21:1344–1348.

    • Search Google Scholar
    • Export Citation
  • SkelhornJ, RuxtonGD. 2011. Context-dependent misclassification of masquerading prey. Evol Ecol. 25:751–761.

  • SkelhornJ, RuxtonGD. 2013. Size-dependent microhabitat selection by masquerading prey. Behav Ecol. 24:89–97.

  • SmithAP. 1986. Ecology of leaf color polymorphism in a tropical forest species: habitat segregation and herbivory. Oecologia. 69:283–287.

    • Search Google Scholar
    • Export Citation
  • SoltauU, DötterlS, Liede-SchumannS. 2009. Leaf variegation in Caladium steudneriifolium (Araceae): a case of mimicry? Evol Ecol. 23:503–512.

    • Search Google Scholar
    • Export Citation
  • SpeedMP, RuxtonGD. 2005. Warning displays in spiny animals: one (more) evolutionary route to aposematism. Evolution. 59:2499–2508.

  • TsukayaH, OkadaH, MohamedM. 2004. A novel feature of structural variegation in leaves of the tropical plant Schismatoglottis calyptrata. J Plant Res. 117:477–480.

    • Search Google Scholar
    • Export Citation
  • TutinTG. 1976. Flora Europaea. Vol. 4. Cambridge: Cambridge University Press.

  • WaageJK. 1981. How the zebra got its stripes - biting flies as selective agents in the evolution of zebra coloration. J Entomol Soc South Africa. 44:351–358.

    • Search Google Scholar
    • Export Citation
  • WilkinsonN. 1969. A brush with life. London: Seeley Service & Co.

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