Dispersing away from bad genotypes: the evolution of Fitness-Associated Dispersal (FAD) in homogeneous environments

BMC Evolutionary Biology

Lilach Hadany²  Yoav Ram²  Amir Ayali¹  Ariel Gueijman² 

[1] Department of Zoology, Tel Aviv University, Tel-Aviv 69978, Israel;Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel-Aviv 69978, Israel

关键词: Stochastic simulations;    Partial migration;    Condition-dependent dispersal;    Fitness-dependent dispersal;    Stress-induced variation;    Outcrossing;    Genetic mixing;    Phenotypic plasticity;   

Others  :  1087071
DOI  :  10.1186/1471-2148-13-125

 received in 2013-01-29, accepted in 2013-05-15,  发布年份 2013

【 摘 要 】

Background

Dispersal is a major factor in ecological and evolutionary dynamics. Although empirical evidence shows that the tendency to disperse varies among individuals in many organisms, the evolution of dispersal patterns is not fully understood. Previous theoretical studies have shown that condition-dependent dispersal may evolve as a means to move to a different environment when environments are heterogeneous in space or in time. However, dispersal is also a means to genetically diversify offspring, a genetic advantage that might be particularly important when the individual fitness is low. We suggest that plasticity in dispersal, in which fit individuals are less likely to disperse (Fitness-Associated Dispersal, or FAD), can evolve due to its evolutionary advantages even when the environment is homogeneous and stable, kin competition is weak, and the cost of dispersal is high.

Results

Using stochastic simulations we show that throughout the parameter range, selection favors FAD over uniform dispersal (in which all individuals disperse with equal probability). FAD also has significant long-term effects on the mean fitness and genotypic variance of the population.

Conclusions

We show that FAD evolves under a very wide parameter range, regardless of its effects on the population mean fitness. We predict that individuals of low quality will have an increased tendency for dispersal, even when the environment is homogeneous, there is no direct competition with neighbors, and dispersal carries significant costs.

【 授权许可】

   
2013 Gueijman et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Bonte D, Van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, et al.: Costs of dispersal. Biol Rev Camb Philos Soc 2012, 87(2):290-312.
• [2]Gadgil M: Dispersal – population consequences and evolution. Ecology 1971, 52(2):253-261.
• [3]Comins HN, Hamilton WD, May RM: Evolutionarily stable dispersal strategies. J Theor Biol 1980, 82(2):205-230.
• [4]Roff DA: The evolution of flightlessness in insects. Ecol Monograph 1990, 60(4):389-421.
• [5]Hamilton WD, May RM: Dispersal in stable habitats. Nature 1977, 269(5629):578-581.
• [6]Hanski I: Single-species metapopulation dynamics – concepts, models and observations. Biol J Linnean Soc 1991, 42(1–2):17-38.
• [7]Vuilleumier S, Perrin N: Effects of cognitive abilities on metapopulation connectivity. Oikos 2006, 113(1):139-147.
• [8]Frank SA: Dispersal polymorphisms in subdivided populations. J Theor Biol 1986, 122(3):303-309.
• [9]Bengtsson BO: Avoiding inbreeding – at what cost. J Theor Biol 1978, 73(3):439-444.
• [10]May RM: When to be incestuous. Nature 1979, 279(5710):192-194.
• [11]Waser PM, Austad SN, Keane B: When should animals tolerate inbreeding. Amer Nat 1986, 128(4):529-537.
• [12]Johnson ML, Gaines MS: Evolution of dispersal – theoretical-models and empirical test using birds and mammals. Annu Rev Ecol Syst 1990, 21:449-480.
• [13]Motro U: Avoiding inbreeding and sibling competition – the evolution of sexual dimorphism for dispersal. Amer Nat 1991, 137(1):108-115.
• [14]Gandon S: Kin competition, the cost of inbreeding and the evolution of dispersal. J Theor Biol 1999, 200(4):345-364.
• [15]Roze D, Rousset F: Inbreeding depression and the evolution of dispersal rates: a multilocus model. Amer Nat 2005, 166(6):708-721.
• [16]Perrin N, Goudet J: Inbreeding, kinship, and the evolution of natal dispersal. In Dispersal. Edited by Clobert J, Danchin E, Dhondt AA, Nichols JD. Oxford: Oxford University Press; 2001:123-142.
• [17]Bowler DE, Benton TG: Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev Camb Philos Soc 2005, 80(2):205-225.
• [18]Ronce O: How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Syst 2007, 38:231-253.
• [19]Clobert J, Le Galliard J-F, Cote J, Meylan S, Massot M: Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 2009, 12(3):197-209.
• [20]Edelaar P, Bolnick DI: Non-random gene flow: an underappreciated force in evolution and ecology. Trends Ecol Evolut 2012, 27(12):659-665.
• [21]Baguette M, Clobert J, Schtickzelle N: Metapopulation dynamics of the bog fritillary butterfly: experimental changes in habitat quality induced negative density-dependent dispersal. Ecography 2011, 34(1):170-176.
• [22]Vercken E, Sinervo B, Clobert J: The importance of a good neighborhood: dispersal decisions in juvenile common lizards are based on social environment. Behav Ecol 2012, 23:1059-1067.
• [23]Donohue K: Setting the stage: Phenotypic plasticity as habitat selection. Int J Plant Sci 2003, 164(3):S79-S92.
• [24]Imbert E, Ronce O: Phenotypic plasticity for dispersal ability in the seed heteromorphic Crepis sancta (Asteraceae). Oikos 2001, 93(1):126-134.
• [25]Wender NJ, Polisetty CR, Donohue K: Density-dependent processes influencing the evolutionary dynamics of dispersal: a functional analysis of seed dispersal in Arabidopsis thaliana (Brassicaceae). Am J Bot 2005, 92(6):960-971.
• [26]Hanski I, Peltonen A, Kaski L: Natal dispersal and social dominance in the common shrew Sorex araneus. Oikos 1991, 62(1):48-58.
• [27]Chaput-Bardy A, Gregoire A, Baguette M, Pagano A, Secondi J: Condition and Phenotype-Dependent Dispersal in a Damselfly. Calopteryx splendens. PLoS One 2010, 5(5):e10694.
• [28]Clarke PMR, Henzi SP, Barrett L, Rendall D: On the road again: competitive effects and condition-dependent dispersal in male baboons. Anim Behav 2008, 76:55-63.
• [29]Solmsen N, Johannesen J, Schradin C: Highly asymmetric fine-scale genetic structure between sexes of African striped mice and indication for condition dependent alternative male dispersal tactics. Mol Ecol 2011, 20(8):1624-1634.
• [30]Shafer ABA, Poissant J, Cote SD, Coltman DW: Does reduced heterozygosity influence dispersal? A test using spatially structured populations in an alpine ungulate. Biol Lett 2011, 7(3):433-435.
• [31]Ims RA, Hjermann DØ: Condition-dependent dispersal. In Dispersal. Edited by Clobert J, Danchin E, Dhondt AA, Nichols JD. Oxford: Oxford University Press; 2001:203-216.
• [32]Ronce O, Isabelle O, Clobert J, Danchin E: Perspectives on the study of dispersal evolution. In Dispersal. Edited by Clobert J, Danchin E, Dhondt AA, Nichols JD. Oxford: Oxford University Press; 2001:341-357.
• [33]Johst K, Brandl R: Evolution of dispersal: the importance of the temporal order of reproduction and dispersal. Proc R Soc Lond B Biol Sci 1997, 264(1378):23-30.
• [34]Travis JMJ, Murrell DJ, Dytham C: The evolution of density–dependent dispersal. Proc R Soc Lond B Biol Sci 1999, 266(1431):1837-1842.
• [35]Poethke HJ, Hovestadt T: Evolution of density-and patch-size-dependent dispersal rates. Proc R Soc Lond B Biol Sci 2002, 269(1491):637-645.
• [36]Weisman S, Shnerb NM, Kessler DA: Evolutionarily Stable Density-Dependent Dispersal. arXiv 2013, 1301:1426.
• [37]Murray BG: Dispersal in vertebrates. Ecology 1967, 48(6):975-978.
• [38]Lawrence WS: Dispesal – an alternative mating tactic condotional on sex-ratio and body size. Behav Ecol Sociobiol 1987, 21(6):367-373.
• [39]Weisser WW: The effects of predation on dispersal. In Dispersal. Edited by Clobert J, Danchin E, Dhondt AA, Nichols JD. Oxford: Oxford University Press; 2001:180-188.
• [40]Poethke Hans J, Weisser Wolfgang W, Hovestadt T: Predator‒Induced Dispersal and the Evolution of Conditional Dispersal in Correlated Environments. Amer Nat 2010, 175(5):577-586.
• [41]Ranta E, Kaitala V: Resource matching and population dynamics in a two-patch system. Oikos 2000, 91(3):507-511.
• [42]Roze D, Rousset F: Strong effects of heterosis on the evolution of dispersal rates. J Evol Biol 2009, 22(6):1221-1233.
• [43]Guillaume F, Perrin N: Joint evolution of dispersal and inbreeding load. Genetics 2006, 173(1):497-509.
• [44]Hadany L, Eshel I, Motro U: No place like home: competition, dispersal and complex adaptation. J Evol Biol 2004, 17(6):1328-1336.
• [45]Gaines MS, McClenaghan LR: Dispersal in Small Mammals. Annu Rev Ecol Syst 1980, 11(1):163-196.
• [46]Greenwood PJ: Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 1980, 28:1140-1162.
• [47]Melosik I: The effect of the ploidy level and genetic background of Sphagnum denticulatum on its morphology and ecological requirements. Oceanol Hydrobiol Stud 2009, 38(4):153-164.
• [48]Selonen V, Hanski IK: Condition‒dependent, phenotype‒dependent and genetic‒dependent factors in the natal dispersal of a solitary rodent. J Anim Ecol 2010, 79(5):1093-1100.
• [49]Edelaar P, Siepielski AM, Clobert J: Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology. Evolution 2008, 62(10):2462-2472.
• [50]Ohta T, Cockerham CC: Detrimental genes with partial selfing and effects on a neutral locus. Gen res 1974, 23(02):191-200.
• [51]Wang J, Hill WG: Effect of selection against deleterious mutations on the decline in heterozygosity at neutral loci in closely inbreeding populations. Genetics 1999, 153(3):1475-1489.
• [52]Pálsson S, Pamilo P: The effects of deleterious mutations on linked, neutral variation in small populations. Genetics 1999, 153(1):475-483.
• [53]Frankham R: Conservation genetics. Annu Rev Genet 1995, 29:305-327.
• [54]Barrett RDH, Schluter D: Adaptation from standing genetic variation. Trends Ecol Evolut 2008, 23(1):38-44.
• [55]Agrawal AF, Hadany L, Otto SP: The evolution of plastic recombination. Genetics 2005, 171(2):803-812.
• [56]Hadany L, Otto SP: The Evolution of Condition-Dependent Sex in the Face of High Costs. Genetics 2007, 176(3):1713-1727.
• [57]Hadany L, Otto SP: Condition-Dependent Sex and the Rate of Adaption. Genetics 2007, 174(S1):S71-78.
• [58]McPeek MA, Holt RD: The evolution of dispersal in aptially and temporally varying environments. Amer Nat 1992, 140(6):1010-1027.
• [59]Armsworth PR, Roughgarden JE: Disturbance induces the contrasting evolution of reinforcement and dispersiveness in directed and random movers. Evolution 2005, 59(10):2083-2096.
• [60]Levin SA, Cohen D, Hastings A: Dispersal strategies in patchy environments. Theor Popul Biol 1984, 26(2):165-191.
• [61]Kisdi E: Dispersal: Risk spreading versus local adaptation. Amer Nat 2002, 159(6):579-596.
• [62]Heino M, Hanski I: Evolution of migration rate in a spatially realistic metapopulation model. Amer Nat 2001, 157(5):495-511.
• [63]Armsworth PR: Conditional dispersal, clines, and the evolution of dispersiveness. Theol Ecol 2009, 2(2):105-117.
• [64]Fretwell SD: Population in a seasonal environment. Princeton, NJ: Princeton University Press; 1972.
• [65]Oro D: Living in a ghetto within a local population: an empirical example of an ideal despotic distribution. Ecology 2008, 89(3):838-846.
• [66]Morris DW, Diffendorfer JE: Reciprocating dispersal by habitat‒selecting white‒footed mice. Oikos 2004, 107(3):549-558.
• [67]Lundberg P, W Morris D: Dispersal among habitats varying in fitness: reciprocating migration through ideal habitat selection. Oikos 2004, 107(3):559-575.
• [68]Rémy A, Galliard L, Gundersen G, Steen H, Andreassen HP: Effects of individual condition and habitat quality on natal dispersal behaviour in a small rodent. J Anim Ecol 2011, 80(5):929-937.
• [69]Calsbeek R, Sinervo B: An experimental test of the ideal despotic distribution. J Anim Ecol 2002, 71(3):513-523.
• [70]Galhardo RS, Hastings PJ, Rosenberg SM: Mutation as a stress response and the regulation of evolvability. Theor PoCrit Rev Biochem Mol Biol pul Biol 2007, 42(5):399-435.
• [71]Ram Y, Hadany L: The evolution of stress-induced hypermutation in asexual populations. Evolution 2012, 66(7):2315-2328.
• [72]Hadany L, Beker T: On the evolutionary advantage of fitness-associated recombination. Genetics 2003, 165(4):2167-2179.
• [73]Zhong WH, Priest NK: Stress-induced recombination and the mechanism of evolvability. Behav Ecol Sociobiol 2011, 65(3):493-502.
• [74]Schoustra S, Rundle HD, Dali R, Kassen R: Fitness-Associated Sexual Reproduction in a Filamentous Fungus. Curr Biol 2010, 20(15):1350-1355.
• [75]Karpestam E, Wennersten L, Forsman A: Matching habitat choice by experimentally mismatched phenotypes. Evol Ecol 2011, 26(4):893-907.
• [76]Holt RD, Barfield M: Habitat selection and niche conservatism. Isr J Ecol Evol 2008, 54(3–4):295-309.
• [77]Roff DA: Population stability and evolution of dispersal in a heterogeneous environment. Oecologia 1975, 19(3):217-237.
• [78]Johnson CA, Fryxell JM, Thompson ID, Baker JA: Mortality risk increases with natal dispersal distance in American martens. Proc R Soc Lond B Biol Sci 2009, 276(1671):3361-3367.
• [79]Hansson B, Westerberg L: On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 2002, 11(12):2467-2474.
• [80]Reed DH, Frankham R: Correlation between fitness and genetic diversity. Conserv Biol 2003, 17(1):230-237.
• [81]Ennos RA: Estimating the relative rates of pollen and seed migration among plant populations. Heredity 1994, 72:250-259.
• [82]Ravigne V, Olivieri I, Gonzalez-Martinez SC, Rousset F: Selective interactions between short-distance pollen and seed dispersal in self-compatible species. Evolution 2006, 60(11):2257-2271.
• [83]Freeman DC, McArthur ED, Harper KT, Blauer AC: Influence of environment on the floral sex-ratio of monoecious plants. Evolution 1981, 35(1):194-197.
• [84]Goldman DA, Willson MF: Sex allocation in functionally hermaphroditic plants – a review and critique. Bot Rev 1986, 52(2):157-194.
• [85]Wise MJ, Coffey LE, Abrahamson WG: Nutrient stress and gall flies interact to affect floral-sex ration in gynomonoecious Solidago altissima (Asteraceae). Am J Bot 2008, 95(10):1233-1239.
• [86]Nathan R: Long-distance dispersal of plants. Science 2006, 313(5788):786-788.
• [87]Armsworth PR, Roughgarden JE: The Structure of Clines with Fitness-Dependent Dispersal. Amer Nat 2008, 172(5):648-657.
• [88]Ruxton GD, Rohani P: Fitness-dependent dispersal in metapopulations and its consequences for persistence and synchrony. J Anim Ecol 1999, 68(3):530-539.
• [89]Armsworth PR, Roughgarden JE: The impact of directed versus random movement on population dynamics and biodiversity patterns. Amer Nat 2005, 165(4):449-465.
• [90]Wright S: Evolution and the genetics of populations: Vol. 2. The theory of gene frequencies. Chicago, IL: Univ. of Chicago Press; 1969.