Disentangling the causes of heterogeneity in male fecundity in gynodioecious Beta vulgaris ssp. maritima

New Phytologist

Volumn 195, Issue 3, 2012, Pages 676-687

  De Cauwer, I ^a,c   Arnaud, J F ^a   Klein, E K ^b   Dufay, M ^a  

^a Univ Lille   (France)

^b INRA   (France)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Cost of restoration; Gynodioecy; Male fecundity; Metapopulation; Pollen dispersal; Polymorphic mating system

Indexed keywords

ALLELE; CYTOPLASM; DICOTYLEDON; DISPERSAL; EVOLUTIONARY BIOLOGY; FECUNDITY; FLOWERING; GYNODIOECY; HERMAPHRODITE; MALE BEHAVIOR; METAPOPULATION; POLLEN; POLYMORPHISM; REPRODUCTIVE COST; REPRODUCTIVE STRATEGY; SEEDLING; STERILITY;

ARTICLE; BEET; BIOLOGICAL MODEL; CYTOPLASM; ECOSYSTEM; GENETIC HETEROGENEITY; GENETIC SELECTION; GENETICS; GENOTYPE; HERMAPHRODITIC SPECIES; PHENOTYPE; PHYSIOLOGY; PLANT INFERTILITY; PLANT SEED; POLLEN; REPRODUCTIVE FITNESS; SELF FERTILIZATION;

BETA VULGARIS; CYTOPLASM; ECOSYSTEM; GENETIC FITNESS; GENETIC HETEROGENEITY; GENOTYPE; HERMAPHRODITIC ORGANISMS; MODELS, BIOLOGICAL; PHENOTYPE; PLANT INFERTILITY; POLLEN; SEEDS; SELECTION, GENETIC; SELF-FERTILIZATION;

BETA VULGARIS; BETA VULGARIS SUBSP. VULGARIS; MAGNOLIOPHYTA;

EID: 84863774802     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04191.x     Document Type: Article

References (48)

1. Adams WT, Birkes D. 1991. Estimating mating patterns in forest tree populations. In: Fineschi S, Malvolti M, Cannata F, Hattemer H, eds. Biochemical markers in the population genetics of forest tree. The Hague, the Netherlands: SPB Academic Publishing, 157-172.
2. Archimowitsch A. 1949. Control of pollination in sugar-beet. Botanical Review 15: 613-628.
3. Austerlitz F, Dick CW, Dutech C, Klein EK, Oddou-Muratorio S, Smouse PE, Sork VL. 2004. Using genetic markers to estimate the pollen dispersal curve. Molecular Ecology 13: 937-954.
4. Bailey MF. 2002. A cost of restoration of male fertility in a gynodioecious species, Lobelia siphilitica. Evolution 56: 2178-2186.
5. Bailey MF, Delph LF, Lively CM. 2003. Modeling gynodioecy: novel scenarios for maintaining polymorphism. American Naturalist 161: 762-776.
6. Boutin V, Jean R, Valero M, Vernet PH. 1988. Gynodioecy in Beta maritima. Acta Oecologica 9: 61-66.
7. Burczyk J, Adams WT, Moran GF, Griffin AR. 2002. Complex patterns of mating revealed in a Eucalyptus regnans seed orchad using allozyme markers and the neighbourhood model. Molecular Ecology 11: 2379-2391.
8. Burczyk J, Prat D. 1997. Male reproductive success in Pseudotsuga menziesii (Mirb.) Franco: the effects of spatial structure and flowering characteristics. Heredity 79: 638-647.
9. Case AL, Caruso CM. 2010. A novel approach to estimating the cost of male fertility restoration in gynodioecious plants. New Phytologist 186: 549-557.
10. del Castillo RF, Trujillo S. 2009. Evidence of restoration cost in the annual gynodioecious Phacelia dubia. Journal of Evolutionary Biology 22: 306-313.
11. Charlesworth D. 1981. A further study of the problem of the maintenance of females in gynodioecious species. Heredity 7: 27-39.
12. Clark JS. 1998. Why trees migrate so fast: confronting theory with dispersal biology and the paleorecord. American Naturalist 152: 204-224.
13. Cuguen J, Wattier R, Saumitou-Laprade P, Forcioli D, Mörchen M, Van Dijk H, Vernet P. 1994. Gynodioecy and mitochondrial DNA polymorphism in natural populations of Beta vulgaris ssp. maritima. Genetics, Selection & Evolution 26: S87-S101.
14. Darwin C. 1877. The different forms of flowers on plants of the same species. London, UK: John Murray.
15. De Cauwer I, Arnaud J-F, Courseaux A, Dufay M. 2011. Gender-specific fitness variation in gynodioecious Beta vulgaris ssp. maritima: do empirical observations fit theoretical predictions? Journal of Evolutionary Biology 24: 2456-2472.
16. De Cauwer I, Arnaud J-F, Schmitt E, Dufay M. 2010a. Pollen limitation of female reproductive success at fine spatial scale in a gynodioecious and wind-pollinated species, Beta vulgaris ssp. maritima. Journal of Evolutionary Biology 23: 2636-2647.
17. De Cauwer I, Dufay M, Cuguen J, Arnaud J-F. 2010b. Effects of fine-scale genetic structure on male mating success in gynodioecious Beta vulgaris ssp. maritima. Molecular Ecology 19: 1540-1558.
18. De Cauwer I, Dufay M, Hornoy B, Courseaux A, Arnaud J-F. 2012. Gynodioecy in structured populations: understanding fine-scale sex ratio variation in gynodioecious Beta vulgaris ssp. maritima. Molecular Ecology 21: 834-850.
19. Delph LF, Touzet P, Bailey MF. 2007. Merging theory and mechanism in studies of gynodioecy. Trends in Ecology & Evolution 22: 17-24.
20. Desplanque B, Viard F, Bernard J, Forcioli D, Saumitou-Laprade P, Cuguen J, Van Dijk H. 2000. The linkage disequilibrium between chloroplast DNA and mitochondrial DNA haplotypes in Beta vulgaris ssp. maritima (L.): the usefulness of both genomes for population genetic studies. Molecular Ecology 9: 141-154.
21. Devaux C, Lavigne C, Falentin-Guyomarc'h H, Vautrin S, Lecomte J, Klein EK. 2005. High diversity of oilseed rape pollen clouds over an agro-ecosystem indicates long-distance dispersal. Molecular Ecology 14: 2269-2280.
22. Dufay M, Cuguen J, Arnaud J-F, Touzet P. 2009. Sex ratio variation among gynodioecious populations of sea beet: can it be explained by negative frequency-dependent selection? Evolution 63: 1483-1497.
23. Dufay M, Pannell JR. 2010. The effect of pollen versus seed flow on the maintenance of nuclear-cytoplasmic gynodioecy. Evolution 64: 772-784.
24. Dufay M, Touzet P, Maurice S, Cuguen J. 2007. Modelling the maintenance of a male fertile cytoplasm in a gynodioecious population. Heredity 99: 349-356.
25. Dufay M, Vaudey V, De Cauwer I, Touzet P, Cuguen J, Arnaud J-F. 2008. Variation in pollen production and pollen viability in natural populations of gynodioecious Beta vulgaris spp. maritima: evidence for a cost of restoration? Journal of Evolutionary Biology 21: 202-212.
26. Ehlers BK, Maurice S, Bataillon T. 2005. Sex inheritance in gynodioecious species: a polygenic view. Proceedings of the Royal Society of London Series B-Biological Sciences 272: 1795-1802.
27. Fénart S, Arnaud J-F, De Cauwer I, Cuguen J. 2008. Nuclear and cytoplasmic genetic diversity in weed beet and sugar beet accessions compared to wild relatives: new insights into the genetic relationships within the Beta vulgaris complex species. Theoretical and Applied Genetics 116: 1063-1077.
28. Fénart S, Austerlitz F, Cuguen J, Arnaud J-F. 2007. Long distance pollen-mediated gene flow at a landscape level: the weed beet as a case study. Molecular Ecology 16: 3801-3813.
29. Fievet V, Touzet P, Arnaud J-F, Cuguen J. 2007. Spatial analysis of nuclear and cytoplasmic DNA diversity in wild sea beet (Beta vulgaris ssp. maritima) populations: do marine currents shape the genetic structure? Molecular Ecology 16: 1847-1864.
30. Gérard PR, Klein EK, Austerlitz F, Fernández-Manjarrés JF, Frascaria-Lacoste N. 2006. Assortative mating and differential male mating success in an ash hybrid zone population. BMC Evolutionary Biology 6: 96.
31. Goto S, Shimatani K, Yoshimaru H, Takahashi Y. 2006. Fat-tailed gene flow in the dioecious canopy tree species Fraxinus mandshurica var. japonica revealed by microsatellites. Molecular Ecology 15: 2985-2996.
32. Gouyon P-H, Vichot F, van Damme JMM. 1991. Nuclear-cytoplasmic male-sterility - Single-point equilibria versus limit-cycles. American Naturalist 137: 498-514.
33. de Haan AA, Hundscheid MPJ, van Hinsberg A. 1997. Effects of CMS types and restorer alleles on plant performance in Plantago lanceolata L.: an indication for cost of restoration. Journal of Evolutionary Biology 10: 803-820.
34. Hardy OJ, Gonzalez-Martinez SC, Fréville H, Boquien G, Mignot A, Colas B, Olivieri I. 2004. Fine-scale genetic structure and gene dispersal in Centaurea corymbosa (Asteraceae) I. Pattern of pollen dispersal. Journal of Evolutionary Biology 17: 795-806.
35. Jones AG, Small CM, Paczolt KA, Ratterman NL. 2010. A practical guide to methods of parentage analysis. Molecular Ecology Resources 10: 6-30.
36. Klein EK, Carpentier FH, Oddou-Muratorio S. 2011. Estimating the variance of male fecundity from genotypes of progeny arrays: evaluation of the Bayesian forward approach. Methods in Ecology and Evolution 2: 349-361.
37. Laporte V, Viard F, Bena G, Valero M, Cuguen J. 2001. The spatial structure of sexual and cytonuclear polymorphism in the gynodioecious Beta vulgaris ssp. maritima: I/at a local scale. Genetics 157: 1699-1710.
38. Larsen K. 1977. Self-incompatibility in Beta vulgaris L. I. Four gametophytic, complementary S-loci in sugar beet. Hereditas 85: 227-248.
39. Letschert JPW. 1993. Beta section Beta : biogeographical patterns of variation and taxonomy. Wageningen Agricultural University Papers 93: 1-137.
40. McCauley DE, Bailey MF. 2009. Recent advances in the study of gynodioecy: the interface of theory and empirism. Annals of Botany (London) 104: 611-620.
41. Meagher TR. 1986. Analysis of paternity within a natural population of Chamaelirium luteum. 1. Identification of most-likely male parents. American Naturalist 128: 199-215.
42. Meier FC, Artschwager E. 1938. Airplane collection of sugar beet pollen. Science 88: 507-508.
43. Oddou-Muratorio S, Klein EK, Austerlitz F. 2005. Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. II. Pollen dispersal and heterogeneity in mating success inferred from parent-offspring analysis. Molecular Ecology 14: 4441-4452.
44. Owen FV. 1942. Inheritance of cross- and self-sterility and self-fertility in Beta vulgaris. Journal of Agricultural Research 64: 679-698.
45. Robledo-Arnuncio JJ, García C. 2007. Estimation of the seed dispersal kernel from exact identification of source plants. Molecular Ecology 16: 5098-5109.
46. Saumitou-Laprade P, Cuguen J, Vernet P. 1994. Cytoplasmic male sterility in plants: molecular evidence and the nucleo-cytoplasmic conflict. Trends in Ecology & Evolution 7: 431-435.
47. Shykoff JA, Kolokotronis SO, Collin CL, Lopez-Villavicencio M. 2003. Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135: 1-9.
48. Torimaru T, Wennström U, Lindgren D, Wang X-R. 2012. Effects of male fecundity, interindividual distance and anisotropic pollen dispersal on mating success in a Scots pine (Pinus sylvestris) seed orchard. Heredity 108: 312-321.