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

Abstract

Abstract. Environmental variation that is not predictably related to cues is expected to drive the evolution of bethedging strategies. The high variance observed in the timing of seed germination has led to it being the most cited diversification strategy in the theoretical bet-hedging literature. Despite this theoretical focus, virtually nothing is known about the mechanisms responsible for the generation of individual-level diversification. Here we report analyses of sources of variation in timing of germination within seasons, germination fraction over two generations and three sequential seasons, and the genetic correlation structure of these traits using almost 10,000 seeds from more than 100 genotypes of the monocarpic perennial Lobelia inflata. Microenvironmental analysis of time to germination suggests that extreme sensitivity to environmental gradients, or microplasticity, even within a homogeneous growth chamber, may act as an effective individual-level diversification mechanism and explains more than 30% of variance in time to germination. The heritability of within-season timing of germination was low (h 2 ϭ 0.07) but significant under homogeneous conditions. Consistent with individual-level diversification, this low h 2 was attributable not to low additive genetic variance, but to an unusually high coefficient of residual variation in time to germination. Despite high power to detect additive genetic variance in within-season diversification, it was low and indistinguishable from zero. Restricted maximum likelihood detected significant genetic variation for germination fraction (h 2 ϭ 0.18) under homogeneous conditions. Unexpectedly, this heritability was positive when measured within a generation by sibling analysis and negative when measured across generations by offspring-on-parent regression. The consistency of dormancy fraction over multiple delays, a major premise of Cohen's classic model, was supported by a strong genetic correlation (r ϭ 0.468) observed for a cohort's germination fraction over two seasons. We discuss implications of the results for the evolution of bet hedging and highlight the need for further empirical study of the causal components of diversification.Key words. Diversification bet hedging, dormancy, environmental unpredictability, heritability, microplasticity, phenotypic plasticity, seed germination. Cole's (1954) renowned result-showing that the fitness of an annual and a perennial plant are equal given that the annual produces just one seed more than the perennialprompted the development of life-history theory by underscoring the evolutionary importance of age(stage)-dependent survival. Mortality at the seed and seedling stage is expected to be much higher than at later stages, especially for annual plants that produce a large number of small seeds (Harper 1977). From the perspective of life-history evolution, the importance of the timing of germination is clear: upon germination, a plant steps from the least to the most vulnerable stage of its life cycle. Thus, the ti...

Response to joint selection on germination and flowering phenology depends on the direction of selection

“…Over both base populations, realized heritability for flowering time (median h 2  = 0.42) was greater than that for germination time (median h 2  = 0.27). Early life cycle traits typically have smaller heritability than those expressed at later stages (reviewed in Geber & Griffen, 2003 [ h 2  = 0.38 flowering time, h 2  = 0.11 germination time]; Simons & Johnston, 2006). Substantial maternal contributions early in the life cycle likely underlie this pattern (Galloway et al., 2009; Wilson & Réale, 2006).…”

Divergent Norms of Reaction to Temperature in Germination Characteristics among Populations of the Arctic-Alpine Annual,Koenigia islandica

“…Regardless, the requirement of high temperatures and light for germination (Wagner and Simons, 2009b), together with the platykurtic distribution of time to germination-seeds of these two populations were still germinating after over a month from imbibition (Fig. 2)-indicate that the populations from Svalbard and Colorado seem to have evolved a ''cautious'' (Schü tz, 2002) or diversified bet-hedging germination strategy (Simons and Johnston, 2006). It also confirms the observations of Amen (1966) and Dorne (1981) that germination generally decreases with increasing severity of the climate.…”

“…In this study we analyze variation in norms of reaction of germination traits among natural populations of an arctic-alpine annual, using seeds produced in the laboratory under uniform conditions to eliminate environmental effects (Quinn and Colosi, 1977;Simons and Johnston, 2006). Loess smoothing techniques (Shipley and Hunt, 1996), were recently introduced for the characterization of complex norms of reaction (Simons and Wagner, 2007) and are used here for this purpose.…”

Greenhouse propagation of the endangered hemiparasiteSchwalbea americana(American chaffseed): experimentation and botanical studies

“…Review of the published literature indicates variation in seed germination requirements, with some studies documenting no seed dormancy (Determann and others 1997;Kirkman and others 1998;Helton and others 2000) and others indicating coldmoist stratification is required to achieve high germination rates (Brumback 1989;Johnson 1995;Obee 1995;Obee and Cartica 1997). Although variation in seed dormancy can be adaptive (Simons and Johnston 2006), the most recent US Fish and Wildlife Service review of this endangered species recommends cold-moist stratification to promote high seed germination rates as the best management practice (USFWS 2008).…”