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Seed dormancy, bet-hedging, and best-bet

September 2nd, 2022 Leave a comment Go to comments

Seed dormancy is a key plant characteristic that occurs among many species worldwide. One mechanism that select for seed dormancy is the bet-hedging strategy. In unpredictable environment (i.e., with high interannual variability) there is a benefit in spreading the germination over a number of years to reduce year-to-year variation in fitness but taking advantage of exceptionally good years for establishment. In those environments, seed dormancy is adaptive; each year there is a small fraction of the seed crop that germinates and the other seeds remain dormant in the soil. Because the environmental conditions of most years are poor, successful establishment only occurs in good (wet) years. Thus bet-hedging selects for seed dormancy and it is a mechanism for living in highly unpredictable environments such as arid ecosystems [1]

There is another environmental setting that also selects for seed dormancy: seasonal (predictable) climate with a dry season during which the vegetation is highly flammable and thus wildfires are frequent (e.g., mediterranean, savanna, warm temperate, and dry boreal ecosystems). In those ecosystems, seed dormancy is adaptive and fire provide both a mechanism for dormancy release (proximate cause) and conditions (postfire) optimal for germination and establishment (low competition, high resource availability, low predation, low pathogen load) that increase fitness and allow maintenance of the population (ultimate cause) [1,2]. Dormant seeds survive the passage of fire and the heat or the chemicals from the combustion (collectively called ‘smoke’ [2,3]) are the stimulus for the seed to recognize a fire gap to germinate. That is, postfire recruitment occurs in a single pulse after fire. Here selection does not favor spreading the risk of recruitment failure over many years (as in the bet-hedging strategy) but, instead, maximizes germination in a single year when conditions are optimal, after fire. We call this strategy the best-bet strategy [1] or environmental matching [2]. This strategy selects for seed dormancy to accumulates seeds in the soil seedbank but also selects for serotiny to accumulate seeds in the canopy seedbank [4]; in both cases, species recruit mostly after fire and not during the interfire period.

There is a further driver that selects for seed dormancy but it does not imply the formation of seed banks (in contrast with bet-hedging and best-bet). Many seeds have acquired seed dormancy to facilitate long-distance dispersal. The clearest example is dispersal by vertebrate frugivores (endozoochory). Frugivores consume the fruit pulp and defaecate or regurgitate the seeds far from the mother plant. This means that seeds need to resist passage through the gut and remain intact until arriving at a new microsite for germination. Thus, seeds of fleshy fruited species typically are dormant, and scarification through the gut releases their dormancy. While bet-hedging spreads germination of seeds over time, this strategy spread the seeds across the space and thus it could be viewed as a spatial bet-hedging strategy.

Figure: Schematic representation of the dynamics of seed recruitment for plants lacking seed dormancy (nondormant; top panel), and for plants with dormant seeds following the bet-hedging strategy (middle panel) and the best-bet strategy (bottom panel). The figure shows the moment of flowering (red asterisk; spring), the germination (black bars; autumn), the seed bank in autumn (empty bars), the recruitment 2 months later (green bars) and the fire (flame; summer). As an example, the seasons are considered as in the Northern Hemisphere, and vertical dotted lines are the end of the year. From [1]
Table: Main characteristics of the evolutionary strategies that select for seed dormancy and seed banks (bet-hedging, best-bet), together with the nondormant strategy.

References

[1] Pausas JG, Lamont BB, Keeley JE., Bond WJ. 2022. Bet-hedging and best-bet strategies shape seed dormancy. New Phytol. [ doi | wiley | pdf]

[2] Pausas JG. & Lamont BB. 2022. Fire-released seed dormancy – a global synthesis. Biol. Rev. 97: 1612-1639. [doi | pdf | supp. mat. | data (figshare)

[3] Keeley JE & Pausas JG. 2018. Evolution of ‘smoke’ induced seed germination in pyroendemic plants. South African J. Bot. 115: 251-255. [doi | pdf]  

[4] Lamont BB, Pausas JG, He T, Witkowski, ETF, Hanley ME. 2020. Fire as a selective agent for both serotiny and nonserotiny over space and time. Critical Rev. Pl. Sci. 39:140-172. [doi | pdf | suppl.]

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