Abstract
Dispersal through space or time (via dormancy) determines gene flow and influences demography. Because of their functional similarities, a covariation between dispersal and dormancy is expected. Dispersal and dormancy are anatomically linked in plants, because they both depend on attributes of the seed, albeit this anatomical association is rarely considered when analyzing interactions between dispersal and dormancy. In this paper, we investigate the extent to which dispersal and dormancy can be expected to correlate and how each might influence adaptation to novel environments such as those brought on by climate change. We review the theoretical and empirical literature on the subject with a focus on seed plants. We find that although a negative correlation between dispersal and dormancy has been theoretically anticipated, several models predict deviations from this expectation under scenarios of environmental heterogeneity. The empirical evidence does not support any specific covariation pattern, likely because the interaction between dispersal and dormancy is affected by multiple environmental and developmental constraints. From a climate change perspective, the effects of dispersal and dormancy on population structure are not equivalent: dormancy-mediated gene flow is intrinsically asymmetric (from the past towards the future) whereas spatial dispersal is not necessarily directional. As a result, selection on traits linked to dormancy and dispersal might differ qualitatively. In particular, gene flow through dormancy can only be adaptive if future environmental conditions are similar to those of the past, or if it contributes to novel allelic combinations. We conclude that, in spite of a long tradition of research, we are unable to anticipate a universal relationship between dispersal and dormancy. More work is needed to predict the relative contributions of spatial dispersal and dormancy to gene flow and adaptation to novel environments.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Baker-Kratz AL, Maguire JD (1984) Germination and dry-matter accumulation in dimorphic achenes of tansy ragwort (Senecio jacobaea). Weed Sci 32:539–545
Baldwin JW, Whitehead SR (2014) Fruit secondary compounds mediate the retention time of seeds in the guts of Neotropical fruit bats. Oecologia 177:453–466. doi:10.1007/s00442-014-3096-2
Barker NP (2005) A review and survey of basicarpy, geocarpy, and amphicarpy in the African and Madagascan flora. Ann Mo Bot Gard 92:445–462
Baskin CC, Baskin JM (2014) Seeds ecology, biogeography and evolution of dormancy and germination. Elsevier, Amsterdam
Boer PJD (1968) Spreading of risk and stabilization of animal numbers. Acta Biotheor 18:165–194. doi:10.1007/BF01556726
Bolmgren K, Eriksson O (2010) Seed mass and the evolution of fleshy fruits in angiosperms. Oikos 119:707–718. doi:10.1111/j.1600-0706.2009.17944.x
Bomblies K, Yant L, Laitinen RA et al (2010) Local-scale patterns of genetic variability, outcrossing, and spatial structure in natural stands of Arabidopsis thaliana. PLoS Genet. doi:10.1371/journal.pgen.1000890
Botkin DB, Saxe H, Araújo MB et al (2007) Forecasting the effects of global warming on biodiversity. Bioscience 57:227–236. doi:10.1641/B570306
Bradshaw WE, Holzapfel CM (2008) Genetic response to rapid climate change: it’s seasonal timing that matters. Mol Ecol 17:157–166. doi:10.1111/j.1365-294X.2007.03509.x
Brancalion PHS, Novembre ADLC, Rodrigues RR, Marcos Filho J (2010) Dormancy as exaptation to protect mimetic seeds against deterioration before dispersal. Ann Bot 105:991–998. doi:10.1093/aob/mcq068
Buoro M, Carlson SM (2014) Life-history syndromes: integrating dispersal through space and time. Ecol Lett 17:756–767. doi:10.1111/ele.12275
Burghardt LT, Metcalf CJE, Wilczek AM et al (2015) Modeling the influence of genetic and environmental variation on the expression of plant life ycles across landscapes. Am Nat. doi:10.1086/679439
Chambers JC, MacMahon JA (1994) A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Trends Ecol Evol 25:263–292
Chen M, MacGregor DR, Dave A et al (2014) Maternal temperature history activates Flowering Locus T in fruits to control progeny dormancy according to time of year. Proc Natl Acad Sci USA 111:18787–18792. doi:10.1073/pnas.1412274111
Cheplick GP (1994) Life history evolution in amphicarpic plants. Plant Species Biol 9:119–131. doi:10.1111/j.1442-1984.1994.tb00092.x
Chiang GCK, Barua D, Kramer EM et al (2009) Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA 106:11661–11666. doi:10.1073/pnas.0901367106
Chiang GCK, Barua D, Dittmar E et al (2013) Pleiotropy in the wild: the dormancy gene DOG1 exerts cascading control on life cycles. Evolution 67:883–893. doi:10.1111/j.1558-5646.2012.01828.x
Christianini AV, Oliveira PS (2010) Birds and ants provide complementary seed dispersal in a neotropical savanna. J Ecol 98:573–582. doi:10.1111/j.1365-2745.2010.01653.x
Chuine I, Beaubien EG (2001) Phenology is a major determinant of tree species range. Ecol Lett 4:500–510. doi:10.1046/j.1461-0248.2001.00261.x
Cipollini ML, Levey DJ (1997) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat 150:346–372. doi:10.1086/286069
Cohen D, Levin SA (1987) The interaction between dispersal and dormancy strategies in varying and heterogeneous environments. In: Teramoto E, Yumaguti M (eds) Mathematical topics in population biology, morphogenesis and neurosciences. Springer, Berlin, pp 110–122
Cohen D, Levin SA (1991) Dispersal in patchy environments: the effects of temporal and spatial structure. Theor Popul Biol 39:63–99. doi:10.1016/0040-5809(91)90041-D
Debeaujon I, Léon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122:403–414. doi:10.1104/pp.122.2.403
Dempster ER (1955) Maintenance of genetic heterogeneity. Cold Spring Harb Symp Quant Biol 20:25–31 (discussion, 31–32)
Donohue K (2002) Germination timing influences natural selection on life-history characters in Arabidopsis thaliana. Ecology 83:1006–1016
Donohue K, de Casas RR, Burghardt L et al (2010) Germination, post-germination adaptation, and species ecological ranges. Annu Rev Ecol Evol Syst 41:293–319. doi:10.1146/annurev-ecolsys-102209-144715
Facelli JM, Chesson P, Barnes N (2005) Differences in seed biology of annual plants in arid lands: a key ingredient of the storage effect. Ecology 86:2998–3006. doi:10.1890/05-0304
Falahati-Anbaran M, Lundemo S, Stenøien HK (2014) Seed dispersal in time can counteract the effect of gene flow between natural populations of Arabidopsis thaliana. New Phytol 202:1043–1054. doi:10.1111/nph.12702
Finch-Savage W, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523
Franks SJ, Sim S, Weis AE (2007) Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc Natl Acad Sci 104:1278–1282. doi:10.1073/pnas.0608379104
Gama-Arachchige NS, Baskin JM, Geneve RL, Baskin CC (2013) Identification and characterization of ten new water gaps in seeds and fruits with physical dormancy and classification of water-gap complexes. Ann Bot 112:69–84. doi:10.1093/aob/mct094
Gardener CJ, McIvor JG, Jansen A (1993a) Passage of legume and grass seeds through the digestive tract of cattle and their survival in faeces. J Appl Ecol 30:63–74. doi:10.2307/2404271
Gardener CJ, McIvor JG, Jansen A (1993b) Survival of seeds of tropical grassland species subjected to bovine digestion. J Appl Ecol 30:75–85. doi:10.2307/2404272
Groszmann M, Bylstra Y, Lampugnani ER, Smyth DR (2010) Regulation of tissue-specific expression of SPATULA, a bHLH gene involved in carpel development, seedling germination, and lateral organ growth in Arabidopsis. J Exp Bot 61:1495–1508. doi:10.1093/jxb/erq015
Harrington GJ, Jaramillo CA (2007) Paratropical floral extinction in the Late Palaeocene-Early Eocene. J Geol Soc 164:323–332. doi:10.1144/0016-76492006-027
Husband BC, Barrett SCH (1996) A metapopulation perspective in plant population biology. J Ecol 84:461–469. doi:10.2307/2261207
Imbert E (2002) Ecological consequences and ontogeny of seed heteromorphism. Perspect Plant Ecol Evol Syst 5:13–36
Imbert E, Escarré J, Lepart J (1999) Local adaptation and non-genetic maternal effects among three populations of Crepis sancta (Asteraceae). Ecoscience 6:223–229
Kalisz S (1986) Variable selection on the timing of germination in Collinsia verna (Scrophulariacea). Evolution 40:479–491
Kidd F, West C (1918) Physiological pre-determination: the influence of the physiological condition of the seed upon the course of subsequent growth and upon the yield II. Review of literature. Chapter I. Ann Appl Biol 5:112–142. doi:10.1111/j.1744-7348.1918.tb05286.x
Kimball S, Angert AL, Huxman TE, Venable DL (2010) Contemporary climate change in the Sonoran Desert favors cold-adapted species. Glob Change Biol 16:1555–1565. doi:10.1111/j.1365-2486.2009.02106.x
Klinkhamer PGL, de Jong TJ, Metz JAJ, Val J (1987) Life history tactics of annual organisms: the joint effects of dispersal and delayed germination. Theor Popul Biol 32:127–156. doi:10.1016/0040-5809(87)90044-X
Kobayashi Y, Yamamura N (2000) Evolution of seed dormancy due to sib competition: effect of dispersal and inbreeding. J Theor Biol 202:11–24
Koenig WD, Knops JMH, Carmen WJ, Sage RD (2009) No trade-off between seed size and number in the Valley Oak Quercus lobata. Am Nat 173:682–688. doi:10.1086/597605
Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226
Larson G, Piperno DR, Allaby RG et al (2014) Current perspectives and the future of domestication studies. Proc Natl Acad Sci 111:6139–6146. doi:10.1073/pnas.1323964111
Lavorel S, Lepart J, Debussche M et al (1994) Small scale disturbances and the maintenance of species diversity in Mediterranean old fields. Oikos 70:455–473
Levey DJ, Byrne MM (1993) Complex ant-plant interactions: rain-forest ants as secondary dispersers and post-dispersal seed predators. Ecology 74:1802–1812. doi:10.2307/1939938
Levin SA, Cohen D, Hastings A (1984) Dispersal strategies in patchy environments. Theor Popul Biol 26:165–191. doi:10.1016/0040-5809(84)90028-5
McCauley DE (2014) What is the influence of the seed bank on the persistence and genetic structure of plant populations that experience a high level of disturbance? New Phytol 202:734–735. doi:10.1111/nph.12732
McPeek MA, Kalisz S (1998) On the joint evolution of dispersal and dormancy in metapopulations. Ergeb Limnol 52:33–51
Menzel A, Sparks TH, Estrella N et al (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1969–1976. doi:10.1111/j.1365-2486.2006.01193.x
Olivieri I (2001) The evolution of seed heteromorphism in a metapopulation: interactions between dispersal and dormancy. pp 245–266
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. doi:10.1146/annurev.ecolsys.37.091305.110100
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. doi:10.1038/nature01286
Peterson AT, Ortega-Huerta MA, Bartley J et al (2002) Future projections for Mexican faunas under global climate change scenarios. Nature 416:626–629. doi:10.1038/416626a
Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253
Saltré F, Saint-Amant R, Gritti ES et al (2013) Climate or migration: what limited European beech post-glacial colonization? Glob Ecol Biogeogr 22:1217–1227. doi:10.1111/geb.12085
Satterthwaite WH (2010) Competition for space can drive the evolution of dormancy in a temporally invariant environment. Plant Ecol 208:167–185. doi:10.1007/s11258-009-9696-y
Schaal BA (1980) Reproductive capacity and seed size in Lupinus texensis. Am J Bot 67:703–709. doi:10.2307/2442663
Snyder RE (2006) Multiple risk reduction mechanisms: can dormancy substitute for dispersal? Ecol Lett 9:1106–1114. doi:10.1111/j.1461-0248.2006.00962.x
Soons MB, Van Der Vlugt C, Van Lith B et al (2008) Small seed size increases the potential for dispersal of wetland plants by ducks. J Ecol 96:619–627. doi:10.1111/j.1365-2745.2008.01372.x
Thiede DA, Augspurger CK (1996) Intraspecific variation in seed dispersion of Lepidium campestre (Brassicaceae). Am J Bot 83:856–866
Thomas CD, Cameron A, Green RE et al (2004) Extinction risk from climate change. Nature 427:145–148. doi:10.1038/nature02121
Traveset A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect Plant Ecol Evol Syst 1(2):151–190
Tsuji N, Yamamura N (1992) A simple evolutionary model of dormancy and dispersal in heterogeneous patches with special reference to phytophagous lady beetles: I. Stable environments. Res Popul Ecol 34:77–90. doi:10.1007/BF02513523
Vander Wall SB, Longland WS (2004) Diplochory: are two seed dispersers better than one? Trends Ecol Evol 19:155–161. doi:10.1016/j.tree.2003.12.004
Venable DL (2007) Bet hedging in a guild of desert annuals. Ecology 88:1086–1090
Venable DL, Brown JS (1988) The selective interactions of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments. Am Nat 131:360–384
Venable DL, Lawlor L (1980) Delayed germination and dispersal in desert annuals—escape in space and time. Oecologia 46:272–282
Vitalis R, Rousset F, Kobayashi Y et al (2013) The joint evolution of dispersal and dormancy in a metapopulation with local extinctions and kin competition. Evolution 67:1676–1691. doi:10.1111/evo.12069
Walther GR, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395
Waser NM, Price MV, Shaw RG (2000) Outbreeding depression varies among cohorts of Ipomopsis aggregata planted in nature. Evolution 54:485–491. doi:10.1111/j.0014-3820.2000.tb00051.x
Wender NJ, Polisetty CR, Donohue K (2005) Density-dependent processes influencing the evolutionary dynamics of dispersal: a functional analysis of seed dispersal in Arabidopsis thaliana (Brassicaceae). Am J Bot 92:960–971
Wiener P, Tuljapurkar S (1994) Migration in variable environments: exploring life-history evolution using structured population models. J Theor Biol 166:75–90. doi:10.1006/jtbi.1994.1006
Wilczek AM, Roe JL, Knapp MC et al (2009) Effects of genetic perturbation on seasonal life history plasticity. Science 323:930–934. doi:10.1126/science.1165826
Wilczek AM, Cooper MD, Korves TM, Schmitt J (2014) Lagging adaptation to warming climate in Arabidopsis thaliana. Proc Natl Acad Sci 111:7906–7913. doi:10.1073/pnas.1406314111
Willis KJ, MacDonald GM (2011) Long-term ecological records and their relevance to climate change predictions for a warmer world. Annu Rev Ecol Evol Syst 42:267–287. doi:10.1146/annurev-ecolsys-102209-144704
Willis CG, Ruhfel B, Primack RB et al (2008) Phylogenetic patterns of species loss in Thoreau’s woods are driven by climate change. Proc Natl Acad Sci USA 105:17029–17033. doi:10.1073/pnas.0806446105
Willis KJ, Bailey RM, Bhagwat SA, Birks HJB (2010a) Biodiversity baselines, thresholds and resilience: testing predictions and assumptions using palaeoecological data. Trends Ecol Evol 25:583–591. doi:10.1016/j.tree.2010.07.006
Willis KJ, Bennett KD, Bhagwat SA, Birks HJB (2010b) 4 °C and beyond: what did this mean for biodiversity in the past? Syst Biodivers 8:3–9. doi:10.1080/14772000903495833
Willis KJ, Bennett KD, Burrough SL et al (2013) Determining the response of African biota to climate change: using the past to model the future. Philos Trans R Soc Lond B Biol Sci 368:20120491. doi:10.1098/rstb.2012.0491
Willis CG, Hall JC, de Casas RR et al (2014) Diversification and the evolution of dispersal ability in the tribe Brassiceae (Brassicaceae). Ann Bot. doi:10.1093/aob/mcu196
Acknowledgments
This work was made possible by the grant “Bet-hedging, trade-offs and the evolution of seed dispersal and dormancy” awarded to R.R.C. by the Talentia program (Junta de Andalucía/FP7) and by a ‘Chercheurs d’Avenir’ grant awarded to P-0. Cheptou from the Region Languedoc-Roussillon. D.L.V. was supported by the NSF Research Grant DEB 1256792.
Author information
Authors and Affiliations
Corresponding author
Additional information
Rafael Rubio de Casas and Kathleen Donohue have contributed equally to this article.
Rights and permissions
About this article
Cite this article
Rubio de Casas, R., Donohue, K., Venable, D.L. et al. Gene-flow through space and time: dispersal, dormancy and adaptation to changing environments. Evol Ecol 29, 813–831 (2015). https://doi.org/10.1007/s10682-015-9791-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-015-9791-6