Skip to main content
SpringerLink
Log in

Drought alters the expression of mating system traits in two species of Clarkia

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Variation in mating system traits can have important consequences for plant populations by affecting reproductive assurance, the expression of inbreeding depression, and the colonization of and persistence in new or altered habitats. Environmental stressors, such as drought, have been hypothesized to induce higher rates of self-fertilization, yet this hypothesis has rarely been tested. Here we measure the response of two sister species of self-compatible annual herbs from contrasting habitats, Clarkia breweri and C. concinna, to an experimentally imposed greenhouse drought treatment. We find that the species differ in their baseline per-flower autogamy rates and the degree of spatial and temporal separation of male and female function within their flowers. Both species show a reduction in temporal separation of anthesis and stigma receptivity with the drought treatment. However, the species from the more mesic habitat, C. concinna, increases its low autogamy rate under drought conditions, whereas the species from the more xeric habitat, C. breweri, decreases its high autogamy rate under drought conditions. Neither species showed a response to drought in flower size or anther-stigma distance. Our results demonstrate that the induction of selfing under environmental stress cannot be assumed and that, in this case, the developmental timing of flower maturation is more plastic than floral morphology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allen GA, Gottlieb LD, Ford VS (1991) Electrophoretic evidence for the independent origins of 2 self-pollinating subspecies of Clarkia concinna (Onagraceae). Can J Bot-Revue Canadienne De Botanique 69:2299–2301

    Article  Google Scholar 

  • Ashman TL, Schoen DJ (1997) The cost of floral longevity in Clarkia tembloriensis: an experimental investigation. Evolut Ecol 11:289–300

    Article  Google Scholar 

  • Baker HG (1955) Self-compatibility and establishment after “long-distance” dispersal. Evolution 9:347–348

    Article  Google Scholar 

  • Barrett SCH, Charlesworth D (1991) Effects of a change in the level of inbreeding on the genetic load. Nature 352:522–524

    Article  PubMed  CAS  Google Scholar 

  • Bolmgren K, Cowan PD (2008) Time— size tradeoffs: a phylogenetic comparative study of flowering time, plant height and seed mass in a north-temperate flora. Oikos 117:424–429

    Article  Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155

    Article  Google Scholar 

  • Campbell DR, Waser NM, Melendez-Ackerman EJ (1997) Analyzing pollinator-mediated selection in a plant hybrid zone: hummingbird visitation patterns on three spatial scales. Am Nat 149:295–315

    Article  Google Scholar 

  • Charlesworth B (1992) Evolutionary rates in partially self-fertilizing species. Am Nat 140:126–148

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Ann Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • Cohen D, Dukas R (1990) The optimal number of female flowers and the fruits-to-flowers ratio in plants under pollination and resource limitation. Am Nat 135:218–241

    Article  Google Scholar 

  • Delesalle VA, Mazer SJ, Paz H (2008) Temporal variation in the pollen: ovule ratios of Clarkia (Onagraceae) taxa with contrasting mating systems: field populations. J Evol Biol 21:310–323

    Google Scholar 

  • Dudley LS, Mazer SJ, Galusky P (2007) The joint evolution of mating system, floral traits and life history in Clarkia (Onagraceae): genetic constraints vs. independent evolution. J Evol Biol 20:2200–2218

    Article  PubMed  CAS  Google Scholar 

  • Eckhart VM, Singh I, Louthan AM et al (2010) Plant-soil water relations and the species border of Clarkia xantiana ssp. xantiana (Onagraceae). Int J Plant Sci 171:749–760

    Article  Google Scholar 

  • Eckhart VM, Geber MA, Morris WF et al (2011) The geography of demography: long-term demographic studies and species distribution models reveal a species border limited by adaptation. Am Nat 178:S26–S43

    Article  PubMed  Google Scholar 

  • Fausto JA, Eckhart VM, Geber MA (2001) Reproductive assurance and the evolutionary ecology of self-pollination in Clarkia xantiana (Onagraceae). Am J Bot 88:1794–1800

    Article  PubMed  Google Scholar 

  • Fishman L, Wyatt R (1999) Pollinator-mediated competition, reproductive character displacement, and the evolution of selfing in Arenaria uniflora (Caryophyllaceae). Evolution 53:1723–1733

    Article  Google Scholar 

  • Goldberg EE, Kohn JR, Lande R et al (2010) Species selection maintains self-incompatibility. Science 330:493–495

    Article  PubMed  CAS  Google Scholar 

  • Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. In Annual Review of Ecology Evolution and Systematics, Annual Review of Ecology Evolution and Systematics, pp 47–79

  • Gottlieb LD, Ford VS (1996) Phylogenetic relationships among the sections of Clarkia (Onagraceae) inferred from the nucleotide sequences of PgiC. Syst Bot 21:45–62

    Article  Google Scholar 

  • Gottlieb LD, Weeden NF (1979) Gene duplication and phylogeny in Clarkia. Evolution 33:1024–1039

    Article  Google Scholar 

  • Grant V (1981) Plant speciation, 2nd edn. Columbia University Press, New York

    Google Scholar 

  • Groom MJ (1998) Allee effects limit population viability of an annual plant. Am Nat 151:487–496

    Article  PubMed  CAS  Google Scholar 

  • Groom MJ, Preuninger TE (2000) Inbreeding depression is not diminished in isolated subpopulations of Clarkia concinna concinna (Onagraceae). Evol Ecol 14:155–180

    Article  Google Scholar 

  • Holtsford TP, Ellstrand NC (1992) Genetic and environmental variation in floral traits affecting outcrossing rate in Clarkia tembloriensis (Onagraceae). Evolution 46:216–225

    Article  Google Scholar 

  • Kalisz S, Vogler D, Fails B et al (1999) The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae). Am J Bot 86:1239–1247

    Article  PubMed  CAS  Google Scholar 

  • Kalisz S, Vogler DW, Hanley KM (2004) Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430:884–887

    Article  PubMed  CAS  Google Scholar 

  • Kalisz S, Randle A, Chaiffetz D et al (2012) Dichogamy correlates with outcrossing rate and defines the selfing syndrome in the mixed-mating genus Collinsia. Ann Bot 109:571–582

    Article  PubMed  Google Scholar 

  • Karron JD, Ivey CT, Mitchell RJ et al (2012) New perspectives on the evolution of plant mating systems. Ann Bot 109:493–503

    Article  PubMed  Google Scholar 

  • Kulbaba MW, Worley AC (2008) Floral design in Polemonium brandegei (Polemoniaceae): genetic and phenotypic variation under hawkmoth and hummingbird pollination. Int J Plant Sci 169:509–522

    Article  Google Scholar 

  • Lande R, Schemske DW (1985) The evolution of self-fertilization and inbreeding depression in plants 1. Evolution 39:24–40

    Article  Google Scholar 

  • Levin DA (2010) Environment-enhanced self-fertilization: implications for niche shifts in adjacent populations. J Ecol 98:1276–1283

    Article  Google Scholar 

  • Levin DA (2012) Mating system shifts on the trailing edge. Ann Bot 109:613–620

    Article  PubMed  Google Scholar 

  • Lewis H (1955) The genus Clarkia, 20(4). University of California Press, Berkeley and Los Angeles

    Google Scholar 

  • Lewis H (1962) Catastrophic selection as a factor in speciation. Evolution 16:257–271

    Article  Google Scholar 

  • Lewis H (1973) Origin of diploid neospecies in Clarkia. Am Nat 107:161–170

    Article  Google Scholar 

  • Lewis H, Lewis ME (1955) The genus Clarkia, vol 20, no. 4. University of California Press, Berkeley

  • Lloyd DG (1979) Some reproductive factors affecting the selection of self-fertilization in plants. Am Nat 113:67–79

    Article  Google Scholar 

  • Lloyd DG (1992) Self-fertilization and cross-fertilization in plants. II. The selection of self-fertilization. Int J Plant Sci 153:370–380

    Article  Google Scholar 

  • Lloyd DG, Webb CJ (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. I Dichogamy. NZ J Bot 24:135–162

    Article  Google Scholar 

  • Lloyd DG, Yates JMA (1982) Intra-sexual selection and the segregation of pollen and stigmas in hermaphrodite plants, exemplified by Wahlenbergia albomarginata (Campanulaceae). Evolution 36:903–913

    Article  Google Scholar 

  • MacSwain J, Raven PH, Thorp R (1973) Comparative behavior of bees and Onagraceae. IV. Clarkia bees of the western United States. Univ Calif Publ Entomol 70:1–80

    Google Scholar 

  • Martin NH, Willis JH (2007) Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 61:68–82

    Article  PubMed  Google Scholar 

  • Mazer SJ, Paz H, Bell MD (2004) Life history, floral development and mating system in Clarkia xantiana (Onagraceae): do floral and whole-plant rates of development evolve independently. Am J Bot 91:2041–2050

    Article  PubMed  Google Scholar 

  • Mazer SJ, Dudley LS, Hove AA et al (2010) Physiological performance in Clarkia sister taxa with contrasting mating systems: do early-flowering autogamous taxa avoid water stress relative to their pollinator-dependent counterparts? Int J Plant Sci 171:1029–1047

    Article  Google Scholar 

  • Moeller DA, Geber MA, Eckhart VM et al (2012) Reduced pollinator service and elevated pollen limitation at the geographic range limit of an annual plant. Ecology 93:1036–1048

    Article  PubMed  Google Scholar 

  • Moore DM, Lewis H (1965) The evolution of self-pollination in Clarkia xantiana. Evolution 19:104–114

    Article  Google Scholar 

  • Morgan M (1993) Fruit to flower ratios and trade-offs in size and number. Evol Ecol 7:219–232

    Article  Google Scholar 

  • Murren CJ, Dudash MR (2012) Variation in inbreeding depression and plasticity across native and non-native field environments. Ann Bot 109:621–632

    Article  PubMed  CAS  Google Scholar 

  • Nicotra AB, Atkin OK, Bonser SP et al (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692

    Article  PubMed  CAS  Google Scholar 

  • Runions CJ, Geber MA (2000) Evolution of the self-pollinating flower in Clarkia xantiana (Onagraceae). I. Size and development of floral organs. Am J Bot 87:1439–1451

    Article  PubMed  CAS  Google Scholar 

  • Sargent RD, Goodwillie C, Kalisz S et al (2007) Phylogenetic evidence for a flower size and number trade-off. Am J Bot 94:2059–2062

    Article  PubMed  Google Scholar 

  • Schoen DJ, Lloyd DG (1984) The selection of cleistogamy and heteromorphic diaspores. Biol J Linn Soc 23:303–322

    Article  Google Scholar 

  • Sime K, Baldwin I (2003) Opportunistic out-crossing in Nicotiana attenuata (Solanaceae), a predominantly self-fertilizing native tobacco. BMC Ecol 3:6

    Article  PubMed  Google Scholar 

  • Stebbins GL (1957) Self fertilization and population variability in the higher plants. Am Nat 91:337–354

    Article  Google Scholar 

  • Stebbins GL (1974) Flowering plants: evolution above the species level. Belknap Press, Cambridge

    Google Scholar 

  • Steets JA, Ashman TL (2004) Herbivory alters the expression of a mixed-mating system. Am J Bot 91:1046–1051

    Article  PubMed  Google Scholar 

  • Steets JA, Wolf DE, Auld JR et al (2007) The role of natural enemies in the expression and evolution of mixed mating in hermaphroditic plants and animals. Evolution 61:2043–2055

    Article  PubMed  Google Scholar 

  • Sytsma KJ, Gottlieb LD (1986) Chloroplast DNA Evolution and Phylogenetic-Relationships in Clarkia (Onagraceae). Am J Bot 73:788–799

    Google Scholar 

  • van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60

    Article  PubMed  Google Scholar 

  • Via S, Gomulkiewicz R, Dejong G et al (1995) Adaptive phenotypic plasticity—consensus and controversy. Trends Ecol & Evol 10:212–217

    Article  CAS  Google Scholar 

  • Vogler DW, Kalisz S (2001) Sex among the flowers: the distribution of plant mating systems. Evolution 55:202–204

    PubMed  CAS  Google Scholar 

  • Worley AC, Barrett SCH (2000) Evolution of floral display in Eichornia paniculata (Pontideriaceae): direct and correlated responses to selection on flower size and number. Evolution 54:1533–1545

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank J. Velzy and D. Polk for expert plant care, T. Miller for unpublished data, and T. Miller, M. Peterson, and two anonymous reviewers for helpful comments on the manuscript. We dedicate this paper to the memory of Les Gottlieb for his inspiring body of work investigating mechanisms of evolution in Clarkia.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, 1156 High St., Santa Cruz, CA, 95064, USA

    Kathleen M. Kay & Devon A. Picklum

Authors
  1. Kathleen M. Kay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Devon A. Picklum
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kathleen M. Kay.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kay, K.M., Picklum, D.A. Drought alters the expression of mating system traits in two species of Clarkia . Evol Ecol 27, 899–910 (2013). https://doi.org/10.1007/s10682-013-9630-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-013-9630-6

Keywords

Search

Navigation