Pollinator visitation patterns strongly influence among-flower variation in selfing rate.

BACKGROUND AND AIMS Adjacent flowers on Mimulus ringens floral displays often vary markedly in selfing rate. We hypothesized that this fine-scale variation in mating system reflects the tendency of bumble-bee pollinators to probe several flowers consecutively on multiflower displays. When a pollinator approaches a display, the first flower probed is likely to receive substantial outcross pollen. However, since pollen carryover in this species is limited, receipt of self pollen should increase rapidly for later flowers. Here the first direct experimental test of this hypothesis is described. METHODS In order to link floral visitation sequences with selfing rates of individual flowers, replicate linear arrays were established, each composed of plants with unique genetic markers. This facilitated unambiguous assignment of paternity to all sampled progeny. A single wild bumble-bee was permitted to forage on each linear array, recording the order of floral visits on each display. Once fruits had matured, 120 fruits were harvested (four flowers from each of five floral displays in each of six arrays). Twenty-five seedlings from each fruit were genotyped and paternity was unambiguously assigned to all 3000 genotyped progeny. KEY RESULTS The order of pollinator probes on Mimulus floral displays strongly and significantly influenced selfing rates of individual fruits. Mean selfing rates increased from 21 % for initial probes to 78 % for the fourth flower probed on each display. CONCLUSIONS Striking among-flower differences in selfing rate result from increased deposition of geitonogamous (among-flower, within-display) self pollen as bumble-bees probe consecutive flowers on each floral display. The resulting heterogeneity in the genetic composition of sibships may influence seedling competition and the expression of inbreeding depression.

[1]  R. Mitchell,et al.  Interspecific pollinator movements reduce pollen deposition and seed production in Mimulus ringens (Phrymaceae). , 2009, American journal of botany.

[2]  Charles F. Williams Effects of floral display size and biparental inbreeding on outcrossing rates in Delphinium barbeyi (Ranunculaceae). , 2007, American journal of botany.

[3]  Christopher R. Herlihy,et al.  EVOLUTIONARY ANALYSIS OF A KEY FLORAL TRAIT IN AQUILEGIA CANADENSIS (RANUNCULACEAE): GENETIC VARIATION IN HERKOGAMY AND ITS EFFECT ON THE MATING SYSTEM , 2007, Evolution; international journal of organic evolution.

[4]  R. Mitchell,et al.  Multiple pollinator visits to Mimulus ringens (Phrymaceae) flowers increase mate number and seed set within fruits. , 2006, American journal of botany.

[5]  J. Brunet,et al.  IMPACT OF INSECT POLLINATOR GROUP AND FLORAL DISPLAY SIZE ON OUTCROSSING RATE , 2006, Evolution; international journal of organic evolution.

[6]  S. Kalisz,et al.  The Evolutionary Enigma of Mixed Mating Systems in Plants: Occurrence, Theoretical Explanations, and Empirical Evidence , 2005 .

[7]  J. Hamrick,et al.  The Mating System of Verbascum thapsus (Scrophulariaceae): The Effect of Plant Height , 2005, International Journal of Plant Sciences.

[8]  D. Carr,et al.  Effects of herbivory and inbreeding on the pollinators and mating system of Mimulus guttatus (Phrymaceae). , 2005, American journal of botany.

[9]  S. Barrett,et al.  Herkogamy and mating patterns in the self-compatible daffodil Narcissus longispathus. , 2005, Annals of botany.

[10]  R. Mitchell,et al.  Patterns of multiple paternity in fruits of Mimulus ringens (Phrymaceae). , 2005, American journal of botany.

[11]  R. Mitchell,et al.  INTERSPECIFIC COMPETITION FOR POLLINATION LOWERS SEED PRODUCTION AND OUTCROSSING IN MIMULUS RINGENS , 2005 .

[12]  R. Mitchell,et al.  The influence of floral display size on selfing rates in Mimulus ringens , 2004, Heredity.

[13]  John M. Bell,et al.  The influence of Mimulus ringens floral display size on pollinator visitation patterns , 2004 .

[14]  H. Koelewijn Sibling competition, size variation and frequency-dependent outcrossing advantage in Plantago coronopus , 2004, Evolutionary Ecology.

[15]  J. Thomson,et al.  POLLEN TRANSFER BY HUMMINGBIRDS AND BUMBLEBEES, AND THE DIVERGENCE OF POLLINATION MODES IN PENSTEMON , 2003, Evolution; international journal of organic evolution.

[16]  S. Barrett Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[17]  M. Cruzan GENETIC MARKERS IN PLANT EVOLUTIONARY ECOLOGY , 1998 .

[18]  J C Stout,et al.  Floral display size in comfrey, Symphytum officinale L. (Boraginaceae): relationships with visitation by three bumblebee species and subsequent seed set , 1998, Oecologia.

[19]  P. Klinkhamer,et al.  Pollen dynamics of bumble-bee visitation on Echium vulgare , 1997 .

[20]  J. D. Karron,et al.  Outcrossing rates of individual Mimulus ringens genets are correlated with anther–stigma separation , 1997, Heredity.

[21]  A. Snow,et al.  The Ecology of Geitonogamous Pollination , 1996 .

[22]  L. Harder,et al.  Pollen Dispersal and Mating Patterns in Animal-Pollinated Plants , 1996 .

[23]  J. D. Karron,et al.  Comparison of pollinator flight movements and gene dispersal patterns in Mimulus ringens , 1995, Heredity.

[24]  J. D. Karron,et al.  The influence of population density on outcrossing rates in Mimulus ringens , 1995, Heredity.

[25]  L. Harder,et al.  Mating cost of large floral displays in hermaphrodite plants , 1995, Nature.

[26]  M. Macnair,et al.  The effects of floral display size on pollinator service to individual flowers of Myosotis and Mimulus , 1995 .

[27]  W. Morris,et al.  Systematic increase in pollen carryover and its consequences for geitonogamy in plant populations , 1994 .

[28]  L. Harder,et al.  Effects of flower number and position on self-fertilization in experimental populations of Eichhornia paniculata (Pontederiaceae) , 1994 .

[29]  A. Robertson The relationship between floral display size, pollen carryover and geitonogamy in Myosotis colensoi (Kirk) Macbride (Boraginaceae) , 1992 .

[30]  J. Antonovics,et al.  Determinants of outcrossing rate in a predominantly self-fertilizing weed, Datura stramonium (Solanaceae) , 1992 .

[31]  D. G. Lloyd,et al.  Self- and Cross-Fertilization in Plants. II. The Selection of Self- Fertilization , 1992, International Journal of Plant Sciences.

[32]  M. R. Dudash,et al.  MULTIPLE PATERNITY AND SELF‐FERTILIZATION IN RELATION TO FLORAL AGE IN MIMULUS GUTTATUS (SCROPHULARIACEAE) , 1991 .

[33]  K. Holsinger Mass-Action Models of Plant Mating Systems: The Evolutionary Stability of Mixed Mating Systems , 1991, The American Naturalist.

[34]  D. Ehrhardt,et al.  ENHANCEMENT OF INBREEDING DEPRESSION BY DOMINANCE AND SUPPRESSION IN IMPATIENS CAPENSIS , 1990, Evolution; international journal of organic evolution.

[35]  C. Eckert,et al.  14 – Variation and Evolution of Mating Systems in Seed Plants , 1990 .

[36]  B. K. Thompson,et al.  The mating system in sympatric populations of Carduus nutans, C. acanthoides and their hybrid swarms , 1989, Heredity.

[37]  K. Ritland CORRELATED MATINGS IN THE PARTIAL SELFER MIMULUS GUTTATUS , 1989, Evolution; international journal of organic evolution.

[38]  P. Klinkhamer,et al.  Plant size and pollinator visitation in Cynoglossum officinale , 1989 .

[39]  M. Clegg,et al.  First-pollination primacy and pollen selection in the morning glory, Ipomoea purpurea , 1987, Heredity.

[40]  J. Thomson Pollen Transport and Deposition by Bumble Bees in Erythronium: Influences of Floral Nectar and Bee Grooming , 1986 .

[41]  M. A. Farris,et al.  POPULATION DENSITY, OUTCROSSING RATE, AND HETEROZYGOTE SUPERIORITY IN PONDEROSA PINE , 1984, Evolution; international journal of organic evolution.

[42]  J. Hamrick,et al.  Variation in estimates of outcrossing in musk thistle populations , 1984 .

[43]  W. Thomas,et al.  Variation in wild populations of Papaver dubium , 1977, Heredity.

[44]  J. Gale,et al.  Variation in wild populations of Papaver dubium , 1974, Heredity.