The Evolutionary Ecology of Seed Germination of Arabidopsis Thaliana: Variable Natural Selection on Germination Timing

Abstract

Abstract. Germination timing of Arabidopsis thaliana displays strong plasticity to geographic location and seasonal conditions experienced by seeds. We identified which plastic responses were adaptive using recombinant inbred lines in a field manipulation of geographic location (Kentucky, KY; Rhode Island, RI), maternal photoperiod (14-h and 10-h days), and season of dispersal (June and November). Transgressive segregation created novel genotypes that had either higher fitness or lower fitness in certain environments than either parent. Natural selection on germination timing and its variation explained 72% of the variance in fitness among genotypes in KY, 30% in June-dispersed seeds in RI, but only 4% in November-dispersed seeds in RI. Therefore, natural selection on germination timing is an extremely efficient sieve that can determine which genotypes can persist in some locations, and its efficiency is geographically variable and depends on other aspects of life history. We found no evidence for adaptive responses to maternal photoperiod during seed maturation. We did find adaptive plasticity to season of seed dispersal in RI. Seeds dispersed in June postponed germination, which was adaptive, while seeds dispersed in November accelerated germination, which was also adaptive. We also found maladaptive plasticity to geographic location for seeds dispersed in June, such that seeds dispersed in KY germinated much sooner than the optimum time. Consequently, bet hedging in germination timing was favorable in KY; genotypes with more variation in germination timing had higher fitness because greater variation was associated with postponed germination. Selection on germination timing varied across geographic location, indicating that germination timing can be a critical stage in the establishment of genotypes in new locations. The rate of evolution of germination timing may therefore strongly influence the rate at which species can expand their range.Key words. Dormancy, maternal effects, natural selection, phenotypic plasticity, seasonal cues. Timing of seed germination is critical to the lifetime performance of the resulting plant. The conditions that elicit germination are the same conditions with which the young seedlings must contend, and those conditions can determine or predict conditions experienced throughout the life of a plant. Germination timing strongly influences seedling survivorship (Biere 1991;Gross and Smith 1991), total lifetime fitness (Miller 1987;Kalisz 1989;Masuda and Washitani 1992), life-history expression (Chouard 1960;Venable 1985;Kalisz 1989;Kalisz and Wardle 1994;Nordborg and Bergelson 1999;Galloway 2001Galloway , 2002, and selection on postgermination characters (Evans and Cabin 1995;Weinig 2000;Donohue 2002). An appropriate germination response to environmental cues is thereby the first requirement for establishment of plants in a location; before plants can display adaptive phenotypes for any adult character, they must first survive through germination.The timing of seed germination stro...

The roles of genetic drift and natural selection in quantitative trait divergence along an altitudinal gradient in Arabidopsis thaliana

“…This suggests that genetic drift impacted population differentiation in traits expressed in the winter-annual life history but not traits expressed in the summer-annual life history. The summer-annual life history is generally rare in A. thaliana (Donohue, 2005; Montesinos-Navarro et al, 2012) but has recently been described to be the common in high elevation population in Spain (Montesinos-Navarro et al, 2012;Picó, 2012). Our study populations were collected as very small mature plants with only a few siliques suggesting that these plants completed their life cycle within one season (summer-annual) and this is also supported by field experiments recently conducted in the Swiss Alps (N. Quèbre, A. Widmer and S. Karrenberg, unpublished results).…”

“…Populations of A. thaliana from even higher altitudes have been reported from the Eastern part of its distribution range but are largely unknown from the European Alps. Arabidopsis thaliana is an annual species that exhibits either a winterannual life history with flowering after vernalization or a summerannual life history where germination and flowering occur in the same year (Donohue, 2005;Montesinos-Navarro et al, 2012;Picó, 2012). The winter-annual life history is considered to be most common but recent evidence shows that the summer-annual life history is more successful in mountainous regions and that both life histories can be expressed in the same population (Picó, 2012).…”

Environmental and Genetic Sources of Diversification in the Timing of Seed Germination: Implications for the Evolution of Bet Hedging

“…Observed seed germination variance is often explained as a diversification bet-hedging strategy whereby individuals minimize the likelihood of complete reproductive failure by paying a cost in the form of a reduction in expected fitness. Explaining seed trait variance has been, and continues to be, a major concern to those interested in life-history evolution because of the close association between seed traits and fitness (e.g., Cohen 1966;Janzen 1969;Smith and Fretwell 1974;Harper 1977;Marks and Prince 1981;Venable 1985;Kalisz 1986;Michaels et al 1988;Venable and Brown 1988;Westoby et al 1992;Philippi 1993;Rees 1997;Simons and Johnston 2000a;Galloway 2002;Donohue et al 2005;Evans and Dennehy 2005).…”

“…The two most commonly studied seed traits are seed size and the timing of germination, and both have been shown to have important fitness consequences. Seed size affects fecundity (Kalisz 1989) and survival (Galen and Stanton 1991;Simons and Johnston 2000a), the timing of germination influences fecundity (Baskin and Baskin 1972;Marks and Prince 1981;Kalisz 1986; Biere 1991b;Galen and Stanton 1991;Shitaka and Hirose 1993;Donohue et al 2005) and survival (Baskin and Baskin 1972;Marks and Prince 1981; Biere 1991b;Simons and Johnston 2000a), and seed size has an effect on the timing of germination (Schaal …”

Genetic and physiological bases for phenological responses to current and predicted climates

“…Selection experiments under contrasting CO 2 or simulated seasonal conditions have identified distinct genetic responses in Arabidopsis that account for evolutionary changes in flowering time depending on the selection environment (Springer et al 2008;Scarcelli & Kover 2009). The fitness consequences of dormancy characteristics differ between seeds dispersed in autumn and those in spring, and seasonal QTL involved in dormancy response and fitness can also be identified (Donohue et al 2005;Huang et al 2010). Thus, knowledge at the genetic level of the basis of phenological traits, the amount of natural variation in these traits, the effect of season on expression of these traits and their fitness consequences in seasonal environments will be necessary to achieve more accurate predictions of the integrated life-history responses of plants to novel environments.…”