| BMC Evolutionary Biology | |
| Widespread disruptive selection in the wild is associated with intense resource competition | |
| David W Pfennig1  Ryan A Martin2  | |
| [1] Department of Biology, CB#3280, University of North Carolina, Chapel Hill, NC 27599, USA;Present address: Department of Biology, CB#7617, North Carolina State University, Raleigh, NC 27695, USA | |
| 关键词: Quadratic selection; Spadefoot toad; Selection differential; Resource polymorphism; Disruptive selection; Competition; | |
| Others : 1140659 DOI : 10.1186/1471-2148-12-136 |
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| received in 2012-03-19, accepted in 2012-07-19, 发布年份 2012 | |
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【 摘 要 】
Background
Disruptive selection has been documented in a growing number of natural populations. Yet, its prevalence within individual systems remains unclear. Furthermore, few studies have sought to identify the ecological factors that promote disruptive selection in the wild. To address these issues, we surveyed 15 populations of Mexican spadefoot toad tadpoles, Spea multiplicata, and measured the prevalence of disruptive selection acting on resource-use phenotypes. We also evaluated the relationship between the strength of disruptive selection and the intensity of intraspecific competition—an ecological agent hypothesized to be an important driver of disruptive selection.
Results
Disruptive selection was the predominant mode of quadratic selection across all populations. However, a directional component of selection favoring an extreme ecomorph—a distinctive carnivore morph—was also common. Disruptive selection was strongest in populations experiencing the most intense intraspecific competition, whereas stabilizing selection was only found in populations experiencing relatively weak intraspecific competition.
Conclusions
Disruptive selection can be common in natural populations. Intraspecific competition for resources may be a key driver of such selection.
【 授权许可】
2012 Martin and Pfennig; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
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| 20150325074814640.pdf | 666KB | ||
| Figure 3. | 87KB | Image | |
| Figure 2. | 127KB | Image | |
| Figure 1. | 101KB | Image |
【 图 表 】
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【 参考文献 】
- [1]Mather K: Polymorphism as an outcome of disruptive selection. Evolution 1955, 9(1):52-61.
- [2]Rueffler C, Van Dooren TJM, Leimar O, Abrams PA: Disruptive selection and then what? Trends in Ecology and Evolution 2006, 21:238-245.
- [3]Bürger R, Gimelfarb A: The effects of intraspecific competition and stabilizing selection on a polygenic trait. Genetics 2004, 167:1425-1443.
- [4]Smith TB, Skúlason S: Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annu Rev Ecol Syst 1996, 27:111-133.
- [5]Thoday JM: Effects of disruptive selection: experimental production of a polymorphic population. Nature 1958, 181:1124-1125.
- [6]Cooper IA, Gilman RT, Boughman JW: Sexual dimorphism and speciation on two ecological coins: patterns from nature and theoretical predictions. Evolution 2011, 65:2553-2571.
- [7]Van Valen LM: Morphological variation and width of ecological niche. Am Nat 1965, 99:377-390.
- [8]Bolnick DI, Doebeli M: Sexual dimorphism and adaptive speciation: two sides of the same ecological coin. Evolution 2003, 57:2433-2449.
- [9]Dieckmann U, Doebeli M: On the origin of species by sympatric speciation. Nature 1999, 400:354-357.
- [10]Rosenzweig ML: Competitive speciation. Biol J Linn Soc 1978, 10:274-289.
- [11]Maynard Smith J: Disruptive selection, polymorphism and sympatric speciation. Nature 1962, 195:60-62.
- [12]Udovic D: Frequency-dependent selection, disruptive selection, and the evolution of reproductive isolation. Am Nat 1980, 116:621-641.
- [13]Kingsolver JG, Diamond SE: Phenotypic selection in natural populations: what limits directional selection? Am Nat 2011, 177:346-357.
- [14]Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri N, Hill CE, Hoang A, Gilbert P, Beerli P: The strength of phenotypic selection in natural populations. Am Nat 2001, 157:245-261.
- [15]Calsbeek R, Smith TB: Experimentally replicated disruptive selection on performance traits in a Caribbean lizard. Evolution 2008, 62:478-484.
- [16]Cucherousset J, Acou A, Blachet S, Britton JA, Beaumont WRC, Gozlan RE: Fitness consequences of individual specialization in resource use and trophic morphology in European eels. Oecologia 2011, 167:75-84.
- [17]Hendry AP, Huber SK, De Leon LF, Herrel A, Podos J: Disruptive selection in a bimodal population of Darwin's finches. Proceedings of The Royal Society, Series B 2009, 276:753-759.
- [18]Martin RA, Pfennig DW: Disruptive selection in natural populations: the roles of ecological specialization and resource competition. Am Nat 2009, 174:268-281.
- [19]Medel R, Botto-Mahan C, Kalin-Arroyo M: Pollinator-mediated selection on the nectar guide phenotype in the Andean monkey flower, Mimulusluteus. Ecology 2003, 84:1721-1732.
- [20]Smith TB: Disruptive selection and the genetic basis of bill size polymorphism in the African finch Pyrenestes. Nature 1993, 363:618-620.
- [21]Pfennig DW, Rice AM, Martin RA: Field and experimental evidence for competition's role in phenotypic divergence. Evolution 2007, 61:257-271.
- [22]Bolnick DI, Lau OL: Predictable patterns of disruptive selection in stickleback in postglacial lakes. Am Nat 2008, 172:1-11.
- [23]Svanbäck R, Persson L: Population density fluctuations change the selection gradient in Eurasian perch. Am Nat 2009, 173:507-516.
- [24]Duffy MA, Brassil CE, Hall SR, Tessier AJ, Caceres CE, Conner JK: Parasite-mediated disruptive selection in a natural Daphnia population. BMC Evol Biol 2008, 8:80. BioMed Central Full Text
- [25]Doebeli M, Dieckmann U: Evolutionary branching and sympatric speciation caused by different types of ecological interactions. Am Nat 2000, 156(Suppl):77-101.
- [26]Wilson DS, Turelli M: Stable underdominance and the evolutionary invasion of empty niches. Am Nat 1986, 127:835-850.
- [27]Abrams PA, Matsuda H, Harada Y: Evolutionarily unstable fitness maxima and stable fitness minima of continuous traits. Evol Ecol 1993, 7:465-487.
- [28]Antonovics J, Thrall PH: Cost of resistance and the maintenance of genetic polymorphism in host-pathogen systems. Proc R Soc Lond Ser B-Biol Sci 1994, 257:105-110.
- [29]Abrams PA, Rueffler C, Kim G: Determinants of the strength of disruptive and/or divergent selection arising from resource competition. Evolution 2008, 62:1571-1586.
- [30]Ackermann M, Doebeli M: Evolution of niche width and adaptive diversification. Evolution 2004, 58:2599-2612.
- [31]Benkman CW: Are the ratios of bill crossing morphs in crossbills the result of frequency-dependent selection? Evol Ecol 1996, 10:119-126.
- [32]Hulsey CD, Hendrickson DA, de Leon FJG: Trophic morphology, feeding performance and prey use in the polymorphic fish Herichthys minckleyi. Evol Ecol Res 2005, 7:303-324.
- [33]Robinson BW, Wilson DS, Shea GO: Trade-offs of ecological specialization: an intraspecific comparison of pumpkinseed sunfish phenotypes. Ecology 1996, 77:170-178.
- [34]Calsbeek R: Experimental evidence that competition and habitat use shape the individual fitness surface. J Evol Biol 2009, 22:97-108.
- [35]Bolnick DI: Can intraspecific competition drive disruptive selection? An experimental test in natural populations of sticklebacks. Evolution 2004, 58:608-618.
- [36]Levins R: Evolution in changing environments. Princeton University Press, Princeton, N.J.; 1968.
- [37]Paull JS, Martin RA, Pfennig DW: Increased competition as a cost of specialization during the evolution of resource polymorphism. Biol J Linn Socin press
- [38]Day T, Young KA: Competitive and facilitative evolutionary diversification. BioScience 2004, 54:101-109.
- [39]Doebeli M: Adaptive diversification. Princeton University Press, Princeton, NJ; 2011.
- [40]Elmer KR, Lehtonen TK, Kautt AF, Harrod C, Meyer A: Rapid sympatric ecological differentiation of crater lake cichlid fishes within historic times. BMC Biology 2010, 8:60. BioMed Central Full Text
- [41]Hori M: Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 1993, 260:216-219.
- [42]Maret TJ, Collins JP: Ecological origin of morphological diversity: a study of alternative trophic phenotypes in larval salamanders. Evolution 1997, 51:898-905.
- [43]Pfennig DW: Polyphenism in spadefoot toads as a locally adjusted evolutionarily stable strategy. Evolution 1992, 46:1408-1420.
- [44]Svanback R, Bolnick DI: Intraspecific competition drives increased resource use diversity within a natural population. Proceedings of the Royal Society B-Biological Sciences 2007, 274:839-844.
- [45]Bragg AN: Gnomes of the night: the spadefoot toads. University of Pennsylvania Press, Philadelphia, PA; 1965.
- [46]Martin RA, Pfennig DW: Field and experimental evidence that competition and ecological opportunity promote resource polymorphism. Biol J Linn Soc 2010, 100:73-88.
- [47]Ledón-Rettig CC, Pfennig DW: Emerging model systems in eco-evo-devo: the environmentally responsive spadefoot toad. Evolution and Development 2011, 13:391-400.
- [48]Martin RA, Pfennig DW: Evaluating the targets of selection during character displacement. Evolution 2011, 65:2946-2958.
- [49]Pomeroy LV: Developmental polymorphism in the tadpoles of the spadefoot toad Scaphiopus multiplicatus. University of California, Ph.D. diss. Riverside, CA; 1981.
- [50]Pfennig DW: The adaptive significance of an environmentally-cued developmental switch in an anuran tadpole. Oecologia 1990, 85:101-107.
- [51]Pfennig DW: Cannibalistic tadpoles that pose the greatest threat to kin are most likely to discriminate kin. Proceedings of the Royal Society of London, Series B 1999, 266:57-81.
- [52]Martin RA, Pfennig DW: Maternal investment influences expression of resource polymorphism in amphibians: implications for the evolution of novel resource-use phenotypes. PLoS One 2010, 5:e9117.
- [53]Pfennig DW, Rice AM, Martin RA: Ecological opportunity and phenotypic plasticity interact to promote character displacement and species coexistence. Ecology 2006, 87(3):769-779.
- [54]Pfennig KS: Female spadefoot toads compromise on mate quality to ensure conspecific matings. Behav Ecol 2000, 11:220-227.
- [55]Pfennig KS: Population differences in condition-dependent sexual selection may promote divergence in non-sexual traits. Evolutionary Ecology Research 2008, 10:763-773.
- [56]van Doorn GS, Edelaar P, Weissing FJ: On the origin of species by natural and sexual selection. Science 2009, 326:1704-1707.
- [57]Lee HJ, Pittlik S, Jones JC, Salzburger W, Barluenga M, Meyer A: Genetic support for random mating between left and right-mouth morphs in the dimorphic scale-eating cichlid fish Perissodus microlepis from Lake Tanganyika. Journal of Fish Biology 2010, 76(8):1940-1957.
- [58]Raeymaekers JAM, Boisjoly M, Delaire L, Berner D, Räsänen K, Hendry AP: Testing for mating isolation between ecotypes: laboratory experiments with lake, stream and hybrid stickleback. J Evol Biol 2010, 23:2694-2708.
- [59]Simovich MA: Analysis of a hybrid zone between the spadefoot toads Scaphiopus multiplicatus and Scaphiopus bombifrons. University of California, Ph.D. Riverside; 1985.
- [60]Gurevitch J, Morrow LL, Wallace A, Walsh JS: A meta-analysis of competition in field experiments. Am Nat 1992, 140:539-572.
- [61]Dybzinski R, Tilman D: Competition and coexistence in plant communities. In The Princeton guide to ecology. Edited by Levin SA. Princeton University Press, Princeton; 2009:186-195.
- [62]Kingsolver JG, Pfennig DW: Individual-level selection as a cause of Cope's rule of phyletic size increase. Evolution 2004, 58:1608-1612.
- [63]Pfennig KS, Pfennig DW: Character displacement as the 'best of a bad situation': fitness trade-offs resulting from selection to minimize resource and mate competition. Evolution 2005, 59:2200-2208.
- [64]Pfennig DW, Mabry A, Orange D: Environmental causes of correlations between age and size at metamorphosis in Scaphiopus multiplicatus. Ecology 1991, 72:2240-2248.
- [65]Brodie ED: Correlatonal selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 1992, 46:1284-1298.
- [66]Lande R, Arnold SJ: The measurement of selection on correlated characters. Evolution 1983, 37:1220-1226.
- [67]Stinchcombe JR, Agrawal AF, Hohenlohe PA, Arnold SJ, Blows MW: Estimating nonlinear selection gradients using quadratic regression coefficients: double or nothing? Evolution 2008, 62:2435-2440.
- [68]Mitchell-Olds T, Shaw RG: Regression analysis and natural selection: statistical inference and biological interpretation. Evolution 1987, 41:1149-1161.
- [69]Schluter D: Estimating the form of natural selection on a quantitative trait. Evolution 1988, 42:849-861.
- [70]Simms EL: Examining selection on the multivariate phenotype: plant resistance to herbivores. Evolution 1990, 44:1177-1188.
- [71]R Development Core Team: R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna; http://www.R-project.org/ webcite
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