Effects of inbreeding and interpopulation crosses on performance and plasticity of two generations of offspring of a declining grassland plant

American Journal of Botany

Volumn 99, Issue 8, 2012, Pages 1300-1313

  Walisch, Tania J ^a,b   Colling, Guy ^a   Poncelet, Myriam ^a   Matthies, Diethart ^b  

^a MUSÉE NATIONAL D HISTOIRE NATURELLE   (Luxembourg)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Competition; Defoliation; Habitat fragmentation; Heterosis; Inbreeding depression; Nutrient effects; Outbreeding depression; Saxifragaceae; Stress

Indexed keywords

COMPETITION (ECOLOGY); CONSERVATION GENETICS; FERTILIZATION (REPRODUCTION); GENERATION TIME; GRASSLAND; HABITAT FRAGMENTATION; HERB; HETEROSIS; HYBRIDIZATION; INBREEDING DEPRESSION; INTERPOPULATION VARIATION; PHENOTYPIC PLASTICITY; POPULATION DECLINE;

ADAPTATION; ARTICLE; CROSS BREEDING; ENVIRONMENT; ENVIRONMENTAL PROTECTION; FLOWER; GENE FLOW; GENETIC VARIABILITY; GENETICS; HETEROSIS; HETEROZYGOTE; INBREEDING; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; PLANT SEED; POLLEN; POLLINATION; POPULATION GENETICS; REPRODUCTION; REPRODUCTIVE ISOLATION; SAXIFRAGACEAE; TIME;

ADAPTATION, PHYSIOLOGICAL; CONSERVATION OF NATURAL RESOURCES; CROSSES, GENETIC; ENVIRONMENT; FLOWERS; GENE FLOW; GENETIC VARIATION; GENETICS, POPULATION; HETEROZYGOTE; HYBRID VIGOR; INBREEDING; PLANT LEAVES; POLLEN; POLLINATION; REPRODUCTION; REPRODUCTIVE ISOLATION; SAXIFRAGACEAE; SEEDS; STRESS, PHYSIOLOGICAL; TIME FACTORS;

EID: 84865005838     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1100479     Document Type: Article

References (107)

1. AGREN, J., and D. W. SCHEMSKE. 1993. Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia hirsuta and B. semiovata. Evolution 47: 125-135.
2. AGUILAR, R., M. QUESADA, L. ASHWORTH, Y. HERRERIAS-DIEGO, and J. LOBO. 2008. Genetic consequences of habitat fragmentation in plant populations: Susceptible signals in plant traits and methodological approaches. Molecular Ecology 17: 5177-5188.
3. AIZEN, M. A., and P. FEINSINGER. 1994. Habitat fragmentation, native insect pollinators and feral honey bees in Argentine "Chaco Serrano". Ecological Applications 4: 378-392.
4. ANGELONI, F., N. J. OUBORG, and R. LEIMU. 2011. Meta-analysis on the association of population size and life history with inbreeding depression in plants. Biological Conservation 144: 35-43.
5. ARMBRUSTER, P., W. E. BRADSHAW, and C. M. HOLZAPFEL. 1997. Evolution of the genetic architecture underlying fi tness in the pitcher-plant mosquito, Wyeomyia smithii. Evolution 51: 451-458.
6. ARMBRUSTER, P., and D. H. REED. 2005. Inbreeding depression in benign and stressful environments. Heredity 95: 235-242.
7. AULD, J. R., and R. A. RELYEA. 2010. Inbreeding depression in adaptive plasticity under predation risk in a freshwater snail. Biology Letters 6: 222-224.
8. BAWA, K. S. 1974. Breeding systems of tree species of a lowland tropical community. Evolution 28: 85-92.
9. BECKER, U., T. REINHOLD, and D. MATTHIES. 2006. Effects of pollination distance on reproduction and offspring performance in Hypochoeris radicata: Experiments with plants from three European regions. Biological Conservation 132: 109-118.
10. BENJAMINI, Y., and Y. HOCHBERG. 2000. On the adaptive control of the false discovery rate in multiple testing with independent statistics. Journal of Educational and Behavioral Statistics 25: 60-83.
11. BERG, H., U. B ECKER, and D. MATTHIES. 2005. P henotypic plasticity in Carlina vulgaris: Effects of geographical origin, population size, and population isolation. Oecologia 143: 220-231.
12. BROCHMANN, C., and A. HAPNES. 2001. Reproductive strategies in some arctic Saxifraga (Saxifragaceae), with emphasis on the narrow endemic S. svalbardensis and its parental species. Botanical Journal of the Linnean Society 137: 31-49.
13. BYERS, D. L., and D. M. WALLER. 1999. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annual Review of Ecology and Systematics 30: 479-513.
14. CARR, D. E., and M. R. DUDASH. 1997. The effects of fi ve generations of enforced selfi ng on potential male and female function in Mimulus guttatus. Evolution 51: 1797-1807.
15. CARR, D. E., and M. R. DUDASH. 2003. Recent approaches into the genetic basis of inbreeding depression in plants. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 358: 1071-1084.
16. CHARLESWORTH, B., M. T. MORGAN, and D. CHARLESWORTH. 1991. Multilocus models of inbreeding depression with synergistic selection and partial self-fertilization. Genetical Research 57: 177-194.
17. CHARLESWORTH, B., and J. H. WILLIS. 2009. The genetics of inbreeding depression. Nature Reviews Genetics 10: 783-796.
18. CHARLESWORTH, D. 1988. A method for estimating outcrossing rates in natural populations of plants. Heredity 61: 469-471.
19. CHARLESWORTH, D., and B. CHARLESWORTH. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18: 237-268.
20. CHEPTOU, P. O., and K. DONOHUE. 2011. Environment-dependent inbreeding depression: Its ecological and evolutionary signifi cance. New Phytologist 189: 395-407.
21. CRÉMIEUX, L., A. BISCHOFF, H. Mueller-Schaerer, and T. STEINGER. 2010. Gene fl ow from foreign provenances into local plant populations: Fitness consequences and implications for biodiversity restoration. American Journal of Botany 97: 94-100.
22. CRNOKRAK, P., and S. C. H. BARRETT. 2002. Perspective: Purging the genetic load: A review of the experimental evidence. Evolution 56: 2347-2358.
23. DE JONG, T. J., N. M. WASER, and P. G. L. KLINKHAMER. 1993. Geitonogamy-The neglected side of selfi ng. Trends in Ecology & Evolution 8: 321-325.
24. DUDASH, M. R. 1990. Relative fi tness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae)-A comparison in three environments. Evolution 44: 1129-1139.
25. DUDASH, M. R., D. E. CARR, and C. B. FENSTER. 1997. Five generations of enforced selfi ng and outcrossing in Mimulus guttatus: Inbreeding depression variation at the population and family level. Evolution 51: 54-65.
26. DUDASH, M. R., C. J. MURREN, and D. E. CARR. 2005. Using Mimulus as a model system to understand the role of inbreeding in conservation: Genetic and ecological approaches. Annals of the Missouri Botanical Garden 92: 36-51.
27. EDMANDS, S. 1999. Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53: 1757-1768.
28. EDMANDS, S. 2007. Between a rock and a hard place: Evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology 16: 463-475.
29. EDMANDS, S., and J. K. DEIMLER. 2004. Local adaptation, intrinsic coadaptation and the effects of environmental stress on interpopulation hybrids in the copepod Tigriopus californicus. Journal of Experimental Marine Biology and Ecology 303: 183-196.
30. EDMANDS, S., and C. C. TIMMERMAN. 2003. Modeling factors affecting the severity of outbreeding depression. Conservation Biology 17: 883-892.
31. ELLSTRAND, N. C., and D. R. ELAM. 1993. Population genetic consequences of small population size: Implications for plant conservation. Annual Review of Ecology and Systematics 24: 217-242.
32. ERICKSON, D. L., and C. B. FENSTER. 2006. Intraspecifi c hybridization and the recovery of fi tness in the native legume Chamaecrista fasciculata. Evolution 60: 225-233.
33. ESCOBAR, J. S., A. NICOT, and P. DAVID. 2008. The different sources of variation in inbreeding depression, heterosis and outbreeding depression in a metapopulation of Physa acuta. Genetics 180: 1593-1608.
34. FENSTER, C. B., and L. F. G ALLOWAY. 2000. Inbreeding and outbreeding depression in natural populations of Chamaecrista fasciculate (Fabaceae). Conservation Biology 14: 1406-1412.
35. FISCHER, M., and D. MATTHIES. 1997. Mating structure and inbreeding and outbreeding depression in the rare plant Gentianella germanica (Gentianaceae). American Journal of Botany 84: 1685-1692.
36. FISCHER, M., and D. MATTHIES. 1998. Effects of population size on performance in the rare plant Gentianella germanica. Journal of Ecology 86: 195-204.
37. FISCHER, M., M. VAN KLEUNEN, and B. SCHMID. 2000. Genetic allee effects on performance, plasticity and developmental stability in a clonal plant. Ecology Letters 3: 530-539.
38. FOX, C. W. 2005. Problems in measuring among-family variation in inbreeding depression. American Journal of Botany 92: 1929-1932.
39. FOX, C. W., and D. H. REED. 2010. Inbreeding depression increases with maternal age in a seed-feeding beetle. Evolutionary Ecology Research 12: 961-972.
40. FRANCIS, B., M. GREEN, and C. PAYNE. 1993. Glim4: The statistical system for generalized linear interactive modelling. Clarendon Press, Oxford, UK.
41. FRANKHAM, R., J. D. BALLOU, M. D. B. ELDRIDGE, R. C. LACY, K. RALLS, M. R. DUDASH, and C. B. FENSTER. 2011. Predicting the probability of outbreeding depression. Conservation Biology 25: 465-475.
42. GALLOWAY, L. F., and J. R. ETTERSON. 2005. Population differentiation and hybrid success in Campanula americana: Geography and genome size. Journal of Evolutionary Biology 18: 81-89.
43. GLAETTLI, M., and J. GOUDET. 2006. Variation in the intensity of inbreeding depression among successive life-cycle stages and generations in gynodioecious Silene vulgaris (Caryophyllaceae). Journal of Evolutionary Biology 19: 1995-2005.
44. GRINDELAND, J. M. 2008. Inbreeding depression and outbreeding depression in Digitalis purpurea: Optimal outcrossing distance in a tetraploid. Journal of Evolutionary Biology 21: 716-726.
45. GUGERLI, F. 1997. Sexual reproduction in Saxifraga oppositifolia L. and Saxifraga bifl ora All. (Saxifragaceae) in the Alps. International Journal of Plant Sciences 158: 274-281.
46. HANSEN, J. E. L., and U. MOLAU. 1994. Pollination biology, mating system, and seed set in a Danish population of Saxifraga granulata. Nordic Journal of Botany 14: 257-268.
47. HOLDEREGGER, R. 1996. Reproduction of the rare monocarpic species Saxifraga mutata L. Botanical Journal of the Linnean Society 122: 301-313.
48. HOLSINGER, K. E. 1988. Inbreeding depression doesn't matter-The genetic basis of mating-system evolution. Evolution 42: 1235-1244.
49. HOLSINGER, K. E. 1991. Inbreeding depression and the evolution of plant mating systems. Trends in Ecology & Evolution 6: 307-308.
50. HONNAY, O., and H. JACQUEMYN. 2007. Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Conservation Biology 21: 823-831.
51. HONNAY, O., H. J ACQUEMYN, B. B OSSUYT, and M. HERMY. 2005. Forest fragmentation effects on patch occupancy and population viability of herbaceous plant species. New Phytologist 166: 723-736.
52. HUFFORD, K. M., and S. J. MAZER. 2003. Plant ecotypes: Genetic differentiation in the age of ecological restoration. Trends in Ecology & Evolution 18: 147-155.
53. HUSBAND, B. C., and D. W. SCHEMSKE. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 54-70.
54. IGIC, B., R. LANDE, and J. R. KOHN. 2008. Loss of self-incompatibility and its evolutionary consequences. International Journal of Plant Sciences 169: 93-104.
55. JOHNSTON, M. O., and D. J. SCHOEN. 1994. On the measurement of inbreeding depression. Evolution 48: 1735-1741.
56. JOHNSTON, M. O., and D. J. SCHOEN. 1996. Correlated evolution of selffertilization and inbreeding depression: An experimental study of nine populations of Amsinckia (Boraginaceae). Evolution 50: 1478-1491.
57. KALISZ, S. 1989. Fitness consequences of mating system, seed weight, and emergence date in a winter annual, Collinsia verna. Evolution 43: 1263-1272.
58. KELLER, M., J. KOLLMANN, and P. J. EDWARDS. 2000. Genetic introgression from distant provenances reduces fi tness in local weed populations. Journal of Applied Ecology 37: 647-659.
59. KELLER, L. F., and D. M. WALLER. 2002. Inbreeding effects in wild populations. Trends in Ecology & Evolution 17: 230-241.
60. KELLY, J. K. 2005. Family level inbreeding depression and the evolution of plant mating systems. New Phytologist 165: 55-62.
61. KÉRY, M., D. MATTHIES, and H.-H. SPILLMANN. 2000. Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. Journal of Ecology 88: 17-30.
62. KOELEWIJN, H. P. 1998. Effects of different levels of inbreeding on progeny fi tness in Plantago coronopus. Evolution 52: 692-702.
63. KOELEWIJN, H. P., V. KOSKI, and O. SAVOLAINEN. 1999. Magnitude and timing of inbreeding depression in Scots pine (Pinus sylvestris L.). Evolution 53: 758-768.
64. KOLB, A. 2005. Reduced reproductive success and offspring survival in fragmented populations of the forest herb Phyteuma spicatum. Journal of Ecology 93: 1226-1237.
65. KORNECK, D., M. SCHNITTLER, and I. VOLLMER. 1996. Rote Liste der Farnund Blütenpfl anzen (Pteridophyta et Spermatophyta) Deutschlands. Schriftenreihe für Vegetationskunde 28: 21-187.
66. LANDE, R., and D. W. SCHEMSKE. 1985. The evolution of self-fertilization and inbreeding depression in plants. 1. Genetic models. Evolution 39: 24-40.
67. LEIMU, R., P. MUTIKAINEN, J. KORICHEVA, and M. FISCHER. 2006. How general are positive relationships between plant population size, fi tness and genetic variation? Journal of Ecology 94: 942-952.
68. LYNCH, M. 1991. The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45: 622-629.
69. MAYER, S. S., D. CHARLESWORTH, and B. MEYERS. 1996. Inbreeding depression in four populations of Collinsia heterophylla Nutt (Scrophulariaceae). Evolution 50: 879-891.
70. MEIER, C., and R. HOLDEREGGER. 1998. Breeding system, germination, and phenotypic differences among populations of Saxifraga aizoides (Saxifragaceae) at the periphery of its alpine distribution. Nordic Journal of Botany 18: 681-688.
71. MELSER, C., A. BIJLEVELD, and P. G. L. KLINKHAMER. 1999. Late-acting inbreeding depression in both male and female function of Echium vulgare (Boraginaceae). Heredity 83: 162-170.
72. MONTALVO, A. M., S. L. WILLIAMS, K. J. RICE, S. L. BUCHMANN, C. CORY, S. N. HANDEL, G. P. NABHAN, R. PRIMACK, and R. H. ROBICHAUX. 1997. Restoration biology: A population biology perspective. Restoration Ecology 5: 277-290.
73. MOORAD, J. A., and M. J. WADE. 2005. A genetic interpretation of the variation in inbreeding depression. Genetics 170: 1373-1384.
74. MUOLA, A., P. MUTIKAINEN, L. LAUKKANEN, M. LILLEY, and R. LEIMU. 2011. The role of inbreeding and outbreeding in herbivore resistance and tolerance in Vincetoxicum hirundinaria. Annals of Botany 108: 547-555.
75. MUSTAJÄRVI, K., P. SIIKAMAKI, and A. AKERBERG. 2005. Inbreeding depression in perennial Lychnis viscaria (Caryophyllaceae): Effects of population mating history and nutrient availability. American Journal of Botany 92: 1853-1861.
76. MUSTAJÄRVI, K., P. SIIKAMÄKI, and S. RYTKÖNEN. 2001. Consequences of plant population size and density for plant-pollinator interactions and plant performance. Journal of Ecology 89: 80-87.
77. NIKLFELD, H. 1999. Rote Listen gefährdeter Pfl anzen Österreichs. Bundesministerium für Gesundheit und Umweltschutz, Wien, Austria.
78. OWEN, K., G. VAUGHTON, and M. RAMSEY. 2007. Facilitated autogamy and costs of selfi ng in the perennial herb Bulbine bulbosa (Asphodelaceae). International Journal of Plant Sciences 168: 579-585.
79. OZIMEC, B., and B. C. HUSBAND. 2011. Effect of recurrent selfi ng on inbreeding depression and mating system evolution in an autopolyploid plant. Evolution 65: 2038-2049.
80. PEDHAZUR, E. J. 1982. Multiple regression in behavioral research: Explanation and prediction. Holt, Rinehart and Winston, New York, New York, USA.
81. PICO, F. X., N. J. OUBORG, and J. M. VAN GROENENDAEL. 2003. Fitness traits and dispersal ability in the herb Tragopogon pratensis (Asteraceae): Decoupling the role of inbreeding depression and maternal effects. Plant Biology 5: 522-530.
82. PICO, F. X., N. J. OUBORG, and J. M. VAN GROENENDAEL. 2004. Evaluation of the extent of among-family variation in inbreeding depression in the perennial herb Scabiosa columbaria (Dipsacaceae). American Journal of Botany 91: 1183-1189.
83. PIKE, N. 2010. Using false discovery rates for multiple comparisons in ecology and evolution. Methods in Ecology and Evolution 2: 278-282.
84. PLUESS, A. R., and J. STÖCKLIN. 2004. Genetic diversity and fi tness in Scabiosa columbaria in the Swiss Jura in relation to population size. Conservation Genetics 5: 145-156.
85. PRICE, M. V., and N. M. WASER. 1979. Pollen dispersal and optimal outcrossing in Delphinium nelsonii. Nature 277: 294-297.
86. RAMULA, S., E. TOIVONEN, and P. MUTIKAINEN. 2007. Demographic consequences of pollen limitation and inbreeding depression in a gynodioecious herb. International Journal of Plant Sciences 168: 443-453.
87. RICHARDS, C. L., O. BOSSDORF, N. Z. MUTH, J. GUREVITCH, and M. PIGLIUCCI. 2006. Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters 9: 981-993.
88. SCHLICHTING, C. D., and D. A. LEVIN. 1986. Effects of inbreeding on phenotypic plasticity in cultivated Phlox. Theoretical and Applied Genetics 72: 114-119.
89. SCHOEN, D. J. 1983. Relative fi tnesses of selfed and outcrossed progeny in Gilia achilleifolia (Polemoniaceae). Evolution 37: 292-301.
90. SCHULTZ, S. T., and J. H. WILLIS. 1995. Individual variation in inbreeding depression-The roles of inbreeding history and mutation. Genetics 141: 1209-1223.
91. SIH, A., and M. S. BALTUS. 1987. Patch size, pollinator behavior, and pollinator limitation in catnip. Ecology 68: 1679-1690.
92. STEVENS, D. P. 1988. On the gynodioecious polymorphism in Saxifraga granulata L. (Saxifragaceae). Biological Journal of the Linnean Society 35: 15-28.
93. STEVENS, D. P., and A. J. RICHARDS. 1985. Gynodioecy in Saxifraga granulate L. (Saxifragaceae). Plant Systematics and Evolution 151: 43-54.
94. STORFER, A. 1999. Gene fl ow and endangered species translocations: A topic revisited. Biological Conservation 87: 173-180.
95. THIELE, J., T. HANSEN, H. R. SIEGISMUND, and T. P. HAUSER. 2010. Genetic variation of inbreeding depression among fl oral and fi tness traits in Silene nutans. Heredity 104: 52-60.
96. UYENOYAMA, M. K., K. E. HOLSINGER, and D. M. WALLER. 1993. Ecological and genetic factors directing the evolution of self-fertilization. Oxford Surveys in Evolutionary Biology 9: 327-381.
97. VAN TREUREN, R., R. BIJLSMA, W. VAN DELDEN, and N. J. OUBORG. 1991. The signifi cance of genetic erosion in the process of extinction. 1. Genetic differentiation in Salvia pratensis and Scabiosa columbaria in relation to population size. Heredity 66: 181-189.
98. VERGEER, P., E. SONDEREN, and N. J. OUBORG. 2004. Introduction strategies put to the test: Local adaptation versus heterosis. Conservation Biology 18: 812-821.
99. VOLIS, S., and Y. H. ZHANG. 2010. Separating effects of gene fl ow and natural selection along an environmental gradient. Evolutionary Biology 37: 187-199.
100. WAGENIUS, S., H. H. HANGELBROEK, C. E. RIDLEY, and R. G. SHAW. 2010. Biparental inbreeding and interremnant mating in a perennial prairie plant: Fitness consequences for progeny in their fi rst eight years. Evolution 64: 761-771.
101. WASER, N. M., and M. V. PRICE. 1989. Optimal outcrossing in Ipomopsis aggregata seed set and offspring fi tness. Evolution 43: 1097-1109.
102. WASER, N. M., and M. V. PRICE. 1991. Outcrossing distance effects in Delphinium nelsonii: Pollen loads, pollen tubes, and seed set. Ecology 72: 171-179.
103. WASER, N. M., and M. V. PRICE. 1994. Crossing-distance effects in Delphinium nelsonii: Outbreeding and inbreeding depression in progeny fi tness. Evolution 48: 842-852.
104. WILLI, Y., M. V AN KLEUNEN, S. DIETRICH, and M. FISCHER. 2007. Genetic rescue persists beyond fi rst-generation outbreeding in small populations of a rare plant. Proceedings of the Royal Society, B, Biological Sciences 274: 2357-2364.
105. WILLIS, J. H. 1993. Effects of different levels of inbreeding on fi tness components in Mimulus guttatus. Evolution 47: 864-876.
106. WILLIS, J. H. 1999. Inbreeding load, average dominance and the mutation rate for mildly deleterious alleles in Mimulus guttatus. Genetics 153: 1885-1898.
107. YOUNG, A., T. BOYLE, and T. BROWN. 1996. The population genetic consequences of habitat fragmentation for plants. Trends in Ecology & Evolution 11: 413-418.