Joint evolution of seed traits along an aridity gradient: seed size and dormancy are not two...

Joint evolution of seed traits along an aridity gradient: seed sizeand dormancy are not two substitutable evolutionary traits intemporally heterogeneous environment

Sergei Volis1 and Gil Bohrer2

1Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China; 2Department of Civil, Environmental & Geodetic

Engineering, The Ohio State University, Columbus, OH, 43210, USA

Author for correspondence:Sergei VolisTel: +86 871 5223170

Email: [email protected]

Received: 27 August 2012Accepted: 29 September 2012

New Phytologist (2013) 197: 655–667doi: 10.1111/nph.12024

Key words: bet hedging, dormancy,precipitation, seed mass, seed traits, temporalheterogeneity.

Summary

� Seed size and dormancy are reproductive traits that interact as adaptations to environmen-

tal conditions. Here, we explore the evolution of these traits in environments that differ in

overall mean favorability and in the extent of temporal predictability.� Our model simulates a population of annual plants living in a range of environments that

differ in aridity, namely mean annual precipitation and inter-annual variation of this mean pre-

cipitation.� The optimal fitness curve is investigated assuming density dependence, three alternative

hypothetical relationships between seed mass and seed survival in the soil (negative, positive,

and independent of mass), and three alternative relationships between survival in soil and pre-

cipitation (strong and intermediate negative relationships, and no relationship).� Our results show that seed size and dormancy are not two substitutable evolutionary traits;

that specific combinations of these two traits are selected in environments that differ in favor-

ability and temporal predictability; that a certain degree of seed dormancy is advantageous

not only in temporally unpredictable environments but also in temporally predictable environ-

ments with high competition; and that more than one combination of seed size and dormancy

(defined in terms of germination fraction) can be optimal, even in spatially homogeneous

environments, potentially allowing selection for more variation in these traits within and

among species.

Introduction

It is recognized that seed traits are crucial plant adaptations thatinteract to optimize plant fitness under given environmental con-ditions (Cohen, 1966; Venable & Brown, 1988). Therefore, anattempt to understand how different environments select for spe-cific seed traits must be based on the joint evolution of thesetraits. Seed size, dormancy, and dispersal are three traits thatallow plants to adapt to environments that vary in their temporaland spatial heterogeneity. It has been shown that dormancy anddispersal allow spreading of the risk of encountering unfavorableconditions in time and space, respectively (Schupp & Fuentes,1995; Wenny, 2001; Venable, 2007). In this work, we will dis-cuss only the temporal aspects of environmental quality andpredictability. Seed size is positively related to seedling growthand establishment (reviewed in Leishman et al., 2000; Moles &Westoby, 2004). However, larger seed size may be associatedwith a lower probability of escaping pre- and post-dispersal pre-dation (Moegenburg, 1996; Gomez, 2004), or escaping unfavor-able conditions by lower persistence in the soil seed bank(Thompson et al., 1993; Bekker et al., 1998). Larger seeds, being

heavier, can also be dispersed shorter distances from the motherplant compared with smaller seeds of the same shape (Ganeshaiah& Uma Shaanker, 1991; Hedge et al., 1991; Bohrer et al. 2008).The relationship between seed size and seed persistence in the soil,in general, is negative (reviewed in Leishman et al., 2000) becauselarge seeds are preferentially harvested by predators (e.g.Abramsky, 1983) and small seeds can more easily penetrate cracksin the soil or be washed in by rainwater and thus escape post-dispersal predation (Thompson et al., 1993; Bekker et al., 1998).This relationship, however, is not universal (Yu et al., 2007).

Joint evolution of these three traits was investigated in severaltheoretical studies. Venable & Lawlor (1980) and Levin et al.(1984) modeled optimal germination in response to dispersabili-ty under density-independent and density-dependent conditions,respectively, and found substitutable effects of dormancy and dis-persal in a response to high temporal unpredictability. Temple-ton & Levin (1979) and Brown & Venable (1986) modeled jointevolution of dormancy and an abstract suit of traits determiningfitness in a temporally varying environment. They came to a sim-ilar conclusion: an increase in temporal unpredictability leads toan increase in dormancy and an increase in specialization for

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‘good-year conditions’. And, conversely, increasing specializationto ‘good-year conditions’ selects for a more persistent soil seedbank. In addition, Brown & Venable (1986) concluded that,under decreasing environmental favorability, selection operateson non-seed traits until a ‘seed-bank threshold’ is crossed atwhich point seed dormancy becomes selectively advantageousand is selected for. Venable & Brown (1988) explored the selec-tive interaction of the three seed traits in a spatially structuredand temporally varying environment under no frequency or den-sity dependence, with patches experiencing environmental condi-tions independently. They found that dormancy, seed size, anddispersal have positive effects on geometric mean fitness. In otherwords, the optimal fitness in temporally heterogeneous environ-ments can be achieved by an increase in either seed dormancy orseed size, and therefore these traits are substitutable to cope withenvironmental unpredictability. However, in their model fecun-dity was a function of seed size by its interaction with environ-mental favorability (seed size was positively related to fecundityunder unfavorable conditions while the opposite was true underfavorable conditions). The last relationship may not be univer-sally true, because it ignores the positive effect of seed size ongrowth and establishment and, as a result, small-seeded plantswill be outcompeted by large-seeded plants under favorableconditions. In this study, we revisit these conclusions and explorethe evolution of seed dormancy and seed mass in temporally het-erogeneous environments that differ in overall mean favorabilityand in predictability, as expressed by the extent of inter-annualvariation.

Description

Our model simulates a population of annual plants living in anarid environment. The model uses empirically based and realisticassumptions about the environment and its interaction with thethree seed traits. Thus, in our model, environmental favorabilityis determined by the total seasonal precipitation; which, given thecomplete lack of precipitation during the dry season, is also theannual precipitation. Inter-annual variation in total annual pre-cipitation represents temporal heterogeneity. Environments thatare highly heterogeneous in time are less predictable, because inhighly variable environments the information about precipitationthat is available to the annual plant population in the current yearis less indicative of the precipitation in the next year.

We chose an approach of optimization and sensitivity analysis.Under this approach, the mean population size after many gener-ations of a population composed exclusively of individuals of agiven trait or trait combination value(s) (i.e. of a single genotype)is considered as an indication of the genotype fitness. Thus, ourmodel cannot simultaneously estimate the fitness of more thanone genotype in a common environment, as is done in an alterna-tive evolutionary stable strategy (ESS) approach. The ESS waspreviously used by Ellner (1985a,b), Rees (1994), Tielborger &Valleriani (2005) and Satterthwaite (2010) to study the evolu-tionary effects of seed dormancy, and by Kobayashi & Yamamura(2000) to study those of seed dormancy and dispersal. However,the ESS approach is impractical when several axes of continuous

traits are considered simultaneously. Here, we conducted a sensi-tivity analysis of the fitness effect of two interacting continuoustraits: seed mass and seed germination fraction (i.e. dormancy).The analysis was conducted using all combinations of these twotraits within the prescribed ranges under a broad range of environ-mental conditions. The environmental conditions were definedby the two axes – environmental favorability and its predictability.In our simulated semiarid climate conditions of the Mediterra-nean, these two axes corresponded to mean annual precipitationand inter-annual variation in precipitation, respectively.

For simplicity, we assume that the reproductive biomass pro-duced by a plant is fixed (i.e. differences in yield among theplants are solely determined by seedling survival) and is convertedto seed number through the inverse function of seed mass. Fol-lowing Weiner et al. (2001), we assign conventional units (0–1)to measures of mass for ease of interpretation; however, theseunits are essentially arbitrary and should not be taken literally.This relationship between seed mass and number is independentof environmental conditions. We assume that seeds are identicalin shape and therefore seed mass is equivalent to seed size. Severalmechanisms of plant adaptation through seed traits, seed massand dormancy are well accepted in the literature and are listedbelow as model assumptions.

Further model assumptions

Assumption 1: There is a trade-off between the number of seedsand the size of seeds produced for a given amount of availableresources for reproductive allocation A negative correlationbetween seed number and seed weight was detected in studiesencompassing a range of life histories, habitats, and continentalfloras (Stevens, 1932; Primack, 1979; Shipley & Dion, 1992;Greene & Johnson, 1994; Turnbull et al., 1999; Jakobsson &Eriksson, 2000; Aarssen & Jordan, 2001; Henery & Westoby,2001). Those studies where this relationship was estimated quan-titatively found the slope not to differ significantly from �1(Aarssen & Jordan, 2001; Henery & Westoby, 2001).

Assumption 2: Seedlings from larger seeds have a higher proba-bility of establishment in general and under water stress condi-tions in particular Larger seeds usually produce larger and morevigorous seedlings, and an advantage of seedlings originatingfrom large seeds in establishment or survivorship was demon-strated in both species comparisons (Jurado & Westoby, 1992;Leishman & Westoby, 1994; Turnbull et al., 1999; Baralotoet al., 2005; Bruun & Ten Brink, 2008) and intraspecific studies(Lewis & Garcia, 1979; Schaal, 1980; Dolan, 1984; Stanton,1984; Weller, 1985; Marshall, 1986; Wulff, 1986; Seiwa et al.,2002; Baraloto et al., 2005). Larger seeds usually have highergermination percentages, higher or advanced emergence fromdeeper sowing (Harper & Obeid, 1967; Maun & Lapierre, 1973;Schimpf, 1977; Weller, 1985; Wulff, 1986; Gulmon, 1992), andless stringent requirements for emergence with respect to litterand herbaceous cover (Gross, 1984; Winn, 1985; Facelli & Pickett,1991; Molofsky & Augspurger, 1992; Reader, 1993; Bosy &Reader, 1995; Rebollo et al., 2001; Dalling & Hubbell, 2002).

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Large-seeded species survive longer under deep shade thansmall-seeded species (Grime & Jeffrey, 1965; Maranon &Bartolome, 1989; Leishman & Westoby, 1994; Saverimuttu &Westoby, 1996; Westoby et al., 1996; Walters & Reich, 2000).This was attributed by Leishman & Westoby (1994) to either alarger initial energy reserve, which is advantageous in habitatswhere gaps in the canopy are regularly created, or the increasedseedling height, which can be advantageous in habitats with asteep gradient of light such as in herbaceous vegetation or forseeds germinating below litter. Under water stress conditions,intraspecific mortality rates are higher for smaller seedlings(Cook, 1980; Parker, 1982; Wulff, 1986) and larger seed mass ispredicted to be favored as a result of the greater energy reserves,which allow seedlings to produce more extensive root systems toobtain water and to better tolerate drought (Baker, 1972; Wulff,1986; Marshall, 1986; Leishman & Westoby, 1994; Seiwa et al.,2002).

These seed-size effects on seedling growth and establishmentwere found to be important at the early stage of plant develop-ment (Newbery & Newman, 1978; Howell, 1981; Zimmerman& Weis, 1983; Dolan, 1984; Houssard & Escarre, 1991; Wei-ner et al., 1997; Tremayne & Richards, 2000; Walters & Reich,2000; Dalling & Hubbell, 2002), and in some cases to persistbeyond early establishment (Arnott, 1969; Schaal, 1980; Weis,1982; Stanton, 1984; Ellison, 1987; Lloret et al., 1999; Simons& Johnson, 2000; Baraloto et al., 2005; Metz et al., 2010). Thepositive seed-size effect may not be evident under conditions ofextreme hazard, for example, drought, when survival is low forall seed masses.

Assumption 3: Larger seeds have a better chance of success incompetitive environments An overwhelming majority of com-petition studies have reported a positive correlation between seedmass and seedling success in competitive environments, that is,that seedlings from small seeds are poorer competitors (Black,1958; Anderson, 1971; Gross & Werner, 1982; Winn, 1985;McConnaughay & Bazzaz, 1987; Reader, 1993; Rees, 1995;Burke & Grime, 1996; Eriksson, 1999; Jakobsson & Eriksson,2000; Leishman, 2001; Dalling & Hubbell, 2002; Turnbullet al., 2004). Seedling–seedling competition is considered to beimportant for vegetation dynamics in communities dominatedby annual plants, that is, in communities where biomass is pro-duced each year mostly from seeds (Leishman, 2001).

Seedlings from large seeds have a better developed root systemand larger root mass and length, enabling them to reach deepersoil levels. This assumption has strong empirical support (Evans& Etherington, 1991; Jurado & Westoby, 1992; Lloret et al.,1999). In arid environments, the upper 5–10 cm of soil can dryout within 5–25 days after the first effective rain when mass ger-mination of seeds occurs (Noy-Meir, 1973). The initial seedlingsize differences, associated with a difference in root system devel-opment, may allow large-seeded seedlings to survive better theinitial stage of establishment after germination. High seedlingmortality is known for Mediterranean and desert annual plantcommunities (Bartolome, 1979; Rice, 1989; Rebollo et al.,2001).

Assumption 4: Seed dormancy is independent of seedmass This effect was empirically shown by Philippi (1993) inhis study of six winter annuals. This means a lack of developmen-tal (physiological or morphological) interdependence, but doesnot exclude the possibility that a selective trade-off between thetwo traits, such as either increased dispersal or increased dor-mancy, is selected for.

Assumption 5: Survival of seeds in the soil may be dependenton seed mass Because there are conflicting views concerning therelationships between seed mass and persistence in the soil, ourmodel tested the effects of three different relationships: negative,positive, and independent of mass.� Negative relationship – the predominant view is that small seedshave a higher probability of survival in the soil because of apositive correlation between seed mass and risk of seed predation(Mitchell, 1975; Davidson, 1977; Nelson & Chew, 1977; Chew& De Vita, 1980; Abramsky, 1983; Nelson & Johnson, 1983;Napela & Grissell, 1993; Reader, 1993; Fox & Mousseau, 1995;Moegenburg, 1996; Hulme, 1998; Gomez, 2004; Azcarate &Peco, 2006; Traba et al., 2006). Lower post-dispersal survivor-ship of large, as compared with small, seeds is expected becauselarge seeds are more likely to be discovered by predators becausethey are more apparent (Feeny, 1976) and have a lower chance ofpenetrating into the soil profile (Van Tooren, 1988; Chamberset al., 1991; Thompson et al., 1993; Bekker et al., 1998; Holzel& Otte, 2004). A decrease in seed size was shown in several stud-ies to be an evolutionary response to herbivory (Smith, 1970;Davidson et al., 1985; Gomez, 2004). A strong negative correla-tion between seed mass and seed longevity in the soil, indepen-dent of phylogeny and of any relationship with life history, wasreported by Hodkinson et al. (1998). Although a negative corre-lation between seed size and persistence in soil may not hold uni-versally (Yu et al., 2007), it was clearly shown to be the case in astudy of the Mojave Desert flora of California (Price & Joyner,1997), the closest analog to the environmental conditions mod-eled here.� Positive relationship – a positive correlation between seed massand persistence may apply to environmental conditions andecosystems where pathogen infestation, which is more detri-mental for small seeds, outweighs an effect of seed predation byrodents and birds (Yu et al., 2007). This can also be the casewhen seed mass is associated with ease of manipulation (e.g.with thickness of seed cover structures such as the endocarp ortesta) (Lee et al., 1991; Blate et al., 1998). In this case, thelarger the seeds the longer the time that is needed to reach theedible part of the seed (Kaufman & Collier, 1981; Alcantaraet al., 2000)� No relationship – as an intermediate alternative, we also tested ascenario under which seed survival in the soil is independent ofthe seed mass. Such a scenario may, for example, apply to situa-tions in which seeds have tough seed coats and therefore smallseeds survive the conditions in the soil as well as large ones, orcontain features making them unpalatable or poisonous, andtherefore avoid seed predation (Kollmann et al., 1998).


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Assumption 6: Survival of seeds in the soil may be affected bysoil moisture As very little quantitative information is availableabout these relationships, we tested two alternatives.� Negative relationship – survival in the soil is inversely propor-tional to soil moisture. Survival is maximal when the soil is dryduring years with no precipitation and decreases with increases inprecipitation and soil moisture. High soil moisture creates condi-tions favorable for soil fungi and bacteria, thus increasing thechance of seed infestation (Mickelson & Grey, 2006).� No relationship – the negative effect of soil moisture on seedsurvival in the soil can be reduced or avoided by a seed if it pos-sesses a hard impermeable coat. Therefore, as a null hypothesis,we also tested a scenario in which seed persistence in the soil isindependent of precipitation amount.

Model formulation

Our model is based on the approach of Cohen (1966), subse-quently used by Brown & Venable (1986) and Venable & Brown(1988). The model describes the population fitness of an annualplant species in terms of the geometric mean of its population sizeover the last 9000 yr of a 10 000-yr simulation experiment. Atany annual time-step, t, the model calculates the total number ofseeds in a population just before the start of the next growing sea-son, Nt+1, that is, the number of seeds that will be available afterseed production, distribution, and mortality before germination.

Ntþ1 ¼ Nt � G � S � Y þ 1� Gð Þ � V½ � Eqn 1

where the evolutionary traits being tested are G, the fraction ofthe seed bank that germinates each year, and M, the seed mass.The variable environmental forcing is represented by the meanannual precipitation, l [P], and its standard deviation, r[P]. Weran simulations for each combination of G and M values within arelevant range under each of the ranges of mean annual precipita-tion regimes with each of the standard deviation levels. The valueswe used for all parameters in the simulations described here, fol-lowing the formulation detailed below (equations 2-5), are pre-sented in Table 1. Nt is the current seed population size, V is thesurvival fraction in the soil, S is seedling survival after germina-tion and Y is fecundity. These three variables are functions of G,M,Nt and the actual annual precipitation in each year, Pt, as follows:

V, the survival fraction of seeds in the soil:

V ¼ Vmax � cvPt1þ dPV exp IPN bV M � aVð Þ½ � Eqn 2

V is a sigmoid-shaped survival function which is dependent onseed mass, M, with two empirical shape parameters, av and bv.Vmax represents the maximal mean survival-in-soil rate underfavorable conditions; av and bv were parameterized such that theinflection point of the sigmoid will be around the median seedmass (Fig. 1). cv is a parameter describing the sensitivity of sur-vival-in-soil to annual precipitation, Pt. cv was set to 0.004 or0.003 in the set of tests that assumed a negative effect of soilmoisture on survival in soil, and 0 in the set of tests that did not

include this effect. Setting cv to values larger than 0.004 led toalmost complete mortality of the seeds in the soil under theranges of precipitation amounts in our model. dPN is a Kroneckerdelta and used as a switch: dPN = 1 when the modeled relation-ship between seed survival in the soil and seed mass is eitherpositive or negative (as detailed in assumption 5) and dPN = 0 foran independent relationship, in which case the function (Eqn 2)is reduced to V = Vmax� cvPt. In these independent cases, wetested three different fixed mean survival rates in the soil:Vmax = 0.1, 0.5 and 0.9. The formulation is further reduced toV = Vmax when there is no dependence on soil moisture (i.e.cv = 0). We used Vmax = 0.9 in that case. IPV is a sign functionthat corresponds to the type of relationship between mass andsurvival-in-soil: it is +1 for the case of a negative relationship and�1 for a positive relationship (Fig. 1).S, seedling survival:

S ¼ 1

1þ exp � aSM � Pt � bS M þ cSð Þ½ � � dSð Þ½ � Eqn 3

The survival function describes a precipitation, Pt (subscript tindicates a specific year), and a seed mass, M, dependent Weibullfunction with four empirical shape and scale parameters, aS, bS,cS, and dS, which were parameterized such that the shape of thesurvival curve will correspond to observations on seedling survivalof two annual grasses, Avena sterilis and Hordeum spontaneum, insemi-arid and desert conditions (S. Volis, unpublished) and therange will fit the arbitrary mass units. This parameterizationallows spanning of the full range of possible values by changingonlyM while keeping the shape parameters constant (Fig. 2a).Y, the number of seeds produced by a germinated seed (fecun-dity):

Y ¼ aYM

� exp �Nt �by ln Mð Þ þ cy� ��

Eqn 4

Y describes a density-dependent and seed size-dependent yieldfunction of seedlings, which includes both the probability of theseedling survival to maturity and their seed production, where Mis seed mass. ay is an empirical coefficient for the maximal fecun-dity (per unit seed mass) and by and cy are shape parameters forthe density and size dependence of young plants’ survival toreproductive maturity (Fig. 2b).

P, precipitation:

½k� ¼ FFT�1 FFT e�½T�L

� �� e2pi½R�

� �

½P� ¼ ½k� � l½k��

� r½P�r½k�

þ l½P�Eqn 5

[P] is a random vector of actual annual precipitation rates in allyears composed of elements, Pt, of the precipitation in each par-ticular year, t. [T] is a vector of all years (1:10 000). The precipi-tation is calculated as an autocorrelated time series with arandom phase, prescribed autocorrelation time, L (2 yr in thiscase), and prescribed mean and standard deviation. [R] is a vector



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of 10 000 uniform random numbers. [k] is a resulting vector ofrandom autocorrelated values (Bohrer et al., 2007). [k] (in arbi-trary units) is converted to precipitation with a prescribed meanand standard deviation (l[P] and r[P], respectively, in mm yr�1)by normalizing it against its own mean and standard deviation(l[k] and r[k], respectively).

Results and Discussion

Independence of seed survival in the soil from seed mass

When seed survival in the soil is high (90%), large seeds(M > 0.8) with little dormancy (G = 0.86) are selected for, except

for a situation with low and highly variable precipitation:l[P] = 100; r[P] = 40 (Fig. 3, lower panel). In this harsh and tem-porally variable environment, seed dormancy is selected for(G = 0.25), but large seeds still have an advantage over small ones.With increases in environmental favorability, in terms of higherprecipitation and soil moisture with lower variability (l[P] = 220–280; r[P] = 0–20), a second optimal peak arises and approachesin magnitude the peak for large seeds with no dormancy. Thispeak is characterized by small seeds and little dormancy(G = 0.92) (Fig. 3, bottom panel).

An intermediate rate of seed mortality in the soil (0.5) resultsin similar trends for seed mass and dormancy, but the magnitudeof the second peak under favorable conditions is always lower

Table 1 Variable symbols and parameter values used in simulations

Symbol Parameter/variable Value [units] Equation

as Shape parameter for precipitationand size-dependent seedling survival

0.27 3

av Shape parameter for size–survivalin soil relationship

5 2

ay Maximal fecundity in seed mass units 10 4bs Shape parameter for precipitation and

size-dependent seedling survival12.5 3

bv Shape parameter for size–survivalin soil relationship

10 2

by Shape parameter for density dependenceof survival to maturity

4E-5 4

cs Scale parameter for precipitation andsize-dependent seedling survival

4 3

cv Proportionality coefficient for the effect ofprecipitation (soil moisture) on survival in soil

0 – no effect 0.003 – intermediate 0.004 – strong 2

cy Shape parameter for density dependenceof survival to maturity

5.3E-5 4

ds Shape parameter for precipitation andsize-dependent seedling survival

7 3

G Annual germination fraction 0.02 : 1 1IPN Sign of survival-in-soil and seed mass

relationship�1 – positive relationship +1 – negative relationship 2

L Autocorrelation time-scale of randomprecipitation time series

2 [yr] 5

M Seed mass 0.02 : 1 [arbitrary units] 1Nt Number of seeds in the current population [number of seeds] 1Nt+1 Number of seeds after annual seed production [number of seeds] 1[P] Vector of autocorrelated actual annual

precipitation rates[mm] 2, 3, 5

Pt Actual annual precipitation [mm] 2, 3[R] Vector uniform random numbers 0–1 [unitless] 5S Seedling survival Fraction [unitless] 3[T] Time-span vector 1 : 10 000 [yr] 5t Current time-step [yr] 1–5V Survival fraction of seeds in the soil Fraction [unitless] 2Vmax Maximal annual survival in soil 0.9 2Y Number of seeds produced by a germinated

seed (fecundity)Number of seeds 4

[k] Vector of random autocorrelated values Arbitrary [unitless] 5dPN Kronecker delta for size-dependent or -independent

survival in soil0 – size-independent 1 – size-dependent 2

l[P] Mean annual precipitation 100 : 280 [mm] 5l[k] Mean of random vector (for normalization) Arbitrary [unitless] 5r[P] Inter-annual standard deviation of precipitation 0 : 40 [mm] 5r[k] Standard deviation of random vector (for normalization) Arbitrary [unitless] 5





than that of the large seeds with little dormancy (Fig. 3, middlepanel). However, that secondary peak for small seeds is more pro-nounced, indicating a faster reduction in the trait advantagearound the peak itself, with less advantage to intermediate formsbetween the two maxima.

Under low seed survival in the soil (Vmax = 0.1), a single opti-mum exists in all the environments. Large seeds (M > 0.8) withno dormancy are selected for, except for a situation with low andhighly variable precipitation: l[P] = 100;r[P] = 40 (Fig. 3, upperpanel). Under these conditions, the optimal strategy is a

combination of intermediate seed mass, M = 0.6, and germina-tion fraction, G = 0.7.

Negative relationship between seed mass and survival inthe soil

Under no temporal variation, harsh environmental conditions(i.e., a persistently low amount of precipitation: l[P] = 100–120; r[P] = 0–10) select for increased seed mass and a high germi-nation fraction (Fig. 4, lower panel). However, with increasedprecipitation l[P] � 160, production of small seeds becomes asecondary optimal (or near-optimal) strategy. In this environ-ment, the competitive advantage of large seeds over small ones ispartially offset by their reduced survival in the soil. The competi-tive disadvantage of small seeds can be further compensated forby producing greater seed numbers. Because the effect of densitydependence becomes stronger in more favorable environments,the contribution of seeds remaining ungerminated in the soil seedbank and avoiding competition by delaying germination to a lessfavorable year becomes more important (Fig. 4, lower panel).

Temporal unpredictability (i.e., inter-annual variation in pre-cipitation) selects for a decrease in seed mass and stronger dor-mancy (i.e. a decrease in the germination fraction) as comparedwith a constant environment with a single optimum. However,these effects can be observed only when the environment is stress-ful. In environments where precipitation is not strongly limitingsurvival (in our model, these conditions correspond to precipita-tion of > 140 mm yr�1), the effects of decreased predictability arenegligible.

One important difference between the results with negativerelationships between seed mass and survival in the soil (Fig. 4,lower panel) and the scenario in which survival in the soil doesnot depend on seed mass (Fig. 3) is the lack of the secondaryoptimal peak for small seeds in the latter scenario, even in envi-ronments with high uniform survival in the soil and high precipi-tation. Another important difference is that harsh environmentalconditions (low precipitation and high variability) with uniformsurvival select for larger seeds (M = 0.6–1.0, depending onthe uniform survival rate), while conditions with a negative seedsize–survival in soil relationship favor small to intermediate seedmasses (M = 0.3–0.4).

Positive relationship between seed mass and survival in thesoil

When small seeds have a lower probability of survival in the soilthan large ones, large seeds are always selected (Fig. 4, upperpanel). The optimal germination fraction in a temporally invari-ant environment is G =0.86, but when the amount of precipita-tion is low (100 mm or lower in our model), variation inprecipitation selects for seed dormancy. Thus, an optimal strategyin a harsh and unpredictable environment is large seeds with alow germination fraction, 0.23 <G < 0.41 when l[P] = 100 and20 � r[P] � 40. This outcome may apply to a situation inwhich large seeds are preferentially harvested but not consumed,and have higher survival in the new places of storage (Mark &

0 0.2 0.4 0.6 0.8 10

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

Seed mass (M )

Pro

babi

lity

of 1

−yr

sur

viva

l in

soil

Fig. 1 Three types of modeled hypothetical relationships between seedmass (M) and the probability of survival in the soil seed bank for 1 yr:negative (bold solid line), positive (gray solid line), and constant, that is,independent of seed mass (dashed lines). The simulated size-independentsurvival range included low, intermediate and high survival probabilities(0.1, 0.5 and 0.9, shown as light, gray and black dashed lines,respectively).

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 10

0.2

0.4

0.6

0.8

1

Seed mass (M )

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 110

0

101

102

103

Seed mass (M )

Yei

ld

Precip0

100

200

300

Nt0

1

2

3

4

5× 104

See

dlin

g su

rviv

alpr

obab

ility

Fig. 2 Survival sof seedlings as a function of seed mass (M) under differentamounts of precipitation (Precip., gray-scale) (upper panel), and fecundity(seed yield, i.e. number of seeds produced per germinated seed) as afunction of seed size (M) and population density (number of individuals,Nt, gray-scale) (lower panel).



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Olesen, 1996; Bas et al., 2009). For example, many seeds possessadaptations for ant dispersal, and burial by ants provides seedswith a nutrient-rich environment and protects them fromsurface-foraging predators and lethal temperatures during fire(Espadaler & Gomez, 1996; Christian & Stanton, 2004; Garridoet al., 2009).

The most important difference between the outcomes of thenegative and positive relationships between seed mass and persis-tence in the soil is that small seeds with high dormancy arestrongly suboptimal in all cases under the latter hypothetical rela-tionship. While a single optimal peak is observed under the fullrange of precipitation and predictability for the positive relation-ship, for the negative relationship, there is a broad range of possi-ble trait combinations that are similar in fitness under almost thefull range of precipitation and predictability (Fig. 4).

Negative relationship between seed survival in soil and soilmoisture

When soil moisture has an effect on survival of seeds in the soilseed bank, selection is acting against delayed germination(Fig. 5). Therefore, a germination fraction G < 0.8 can beoptimal only if the effect of soil moisture is greatly reduced,that is in xeric environments with low annual precipitation andintermediate to high inter-annual variation in precipitation. Inthis environment, delayed germination was selected for under

both positive and negative relationships between seed mass andsurvival in the soil, and the optimal seed mass corresponded towhether larger or smaller seeds had higher survival in the soil.Under all other environmental conditions, a negative dependencebetween seed mass and survival in the soil led to a single optimalstrategy of large seeds with no dormancy (Fig. 5). This is surpris-ing because, with no dormancy, there should not be an effect ofseed mortality in the soil. This is indeed the case (Fig. 6). Undera negative effect of precipitation on survival in the soil, increasedmortality in the soil in wet years negates the advantage of smallseeds with dormancy. Therefore, with higher mortality in thesoil, the optimal trait combination becomes unimodal favoringlarge seed mass. A high germination fraction is selected for underall environmental conditions except the most limiting and unpre-dictable ones.

These results show that, in xeric temporally fluctuating envi-ronments, a strategy in which some seeds enter the soil seed bankis always advantageous, and the optimal seed mass depends onthe importance of seed predation and/or infestation, the presenceof a hard seed coat, etc. In a species having seeds that are not sub-jected to predation because of some biological features or becausethe granivorous species are absent in the environment theyoccupy, large seeds are selected. However, if these conditions arenot met, a decrease in seed mass becomes important for seedescape from predation. Species having small seeds with no specialadaptations to persist in the soil bank can be highly successful in

Fig. 3 Effect of survival in the soil on fitness (vertical axis, color) under a range of seed mass (M) and germination fraction (G) values, and under high or lowannual precipitation (100 and 280mm, respectively) and a range of precipitation predictability levels (standard deviation in precipitation, Precip. STD = 0;20 and 40, from left to right). Here we assumed that survival in the soil is independent of seed mass and precipitation (mean annual survival rates in the soilare fixed at Vmax = 0.1, 0.5 and 0.9 from top to bottom; see Eqn 2 and Fig 1).





xeric (desert) environments, because even seeds without hardcoats can be well preserved in dry soil.

In Mediterranean conditions where soil moisture is less limit-ing and conditions are more predictable, some degree of dor-mancy can still be advantageous if seeds are well protected fromthe effects of high soil moisture, that is, have a hard impermeablecoat. If predation is strong, species having small seeds with orwithout dormancy can be as successful as species with large non-dormant seeds, but only if they have features allowing toleranceof high soil moisture.

Conclusions

In our study, we investigated how the optimal combination(s) oftwo seed traits, dormancy and size, evolves along the aridity gra-dient, which is characterized by two parameters, the amount ofannual precipitation and its inter-annual variation. In our simula-tions, we tried to embrace a variety of interactions, both bioticand abiotic, between seeds and environment. The complexity ofthe results produced can be summarized as the following keyfindings (Fig. 7).� Α low amount of precipitation selects for dormancy, but onlywhen precipitation fluctuates greatly from year to year. Whenprecipitation is low and temporally predictable, dormancy isalways selected against. Under high precipitation, a high (but not100%) germination fraction is selected for regardless of inter-annual fluctuations in precipitation amount.

� Optimal seed mass depends on a relationship between seedmass and soil moisture, and susceptibility to seed predation andinfestation, in addition to the amount and predictability of rain-fall. Either only large or both small and large seeds can be optimalor nearly optimal under high precipitation regardless of the mag-nitude of inter-annual fluctuations in precipitation. Environ-ments with constantly low precipitation always select for largeseeds, while under low and highly fluctuating precipitation, eithersmall or large seeds can be optimal (Fig. 6).� In productive environments, that is those with high precipita-tion, bimodality is often observed (Fig. 6) with optimal peaksbeing flat and resembling a plateau, while in low-productivityenvironments the peak is always single and narrow.

In this study, we simulated simplistic environmental condi-tions while preserving a natural range of two critical environmen-tal properties, the mean and variability of annual precipitation,representing a gradient of aridity from xeric desert to more mesicMediterranean climates. The typical Mediterranean climate ischaracterized by rainy winters when annual vegetation sprouts,and long dry summers when annual vegetation is present only inthe soil seed banks. The inter-annual precipitation variability andprobability of reproductive failure increase along the gradient ofaridity. Several of our findings correspond well with those ofexperimental studies conducted in this region. The predictionthat small seed mass will be optimal under conditions of low pre-cipitation, low predictability and a negative relationship betweenseed mass and survival in the soil (or constant and low survival in

Fig. 4 Effect of the type of relationship between seed mass and survival in the soil (negative lower panels, positive upper panels) on fitness (vertical axis,color) under a range of seed mass (M) and germination fraction (G) values, and under high or low annual precipitation (100 and 280mm, respectively) anda range of precipitation predictability levels (standard deviation in precipitation, Precip. STD, μ[p] = 0, 20 and 40, from left to right). In all cases we assumedno direct effect of precipitation on survival in soil cv = 0 (Eqn 2).



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NewPhytologist662

the soil) (Fig. 3, upper panel; Fig 4, lower panel) was observed ina comparative study by Harel et al. (2011) and in two annualgrasses (Volis, 2007, 2012). The latter two species also demon-strated a positive relationship between germination fraction andprecipitation predictability at the population location (Voliset al., 2002, 2004; Volis, 2009; Fig. 6).

Our study does not only provide theoretical support foralready known phenomena. In a previous model analyzing theevolution of seed traits in temporally varying environments, seed

mass and dormancy were found to be substitutable traits (Venable& Brown, 1988). The results of our model suggest the opposite;that is, that there is an interaction between these two traits andthis interaction is environment-dependent. Specifically, underdifferent environmental favorability and temporal predictability,different combinations of seed mass and dormancy are selected.Our results also show that several combinations of seed traits (i.e.seeds of a range of sizes with low and high germination fractions)can be optimal or near-optimal in a given spatially homogeneous

Fig. 5 Effect of negative relationship between precipitation and survival in the soil on fitness (vertical axis, color) under a range of seed mass (M) andgermination fraction (G) values, and under high or low annual precipitation (100 and 280mm, respectively) and a range of precipitation predictabilitylevels (standard deviation in precipitation, Precip. STD μ[p] = 0, 20 and 40, from left to right).The lower panels show the results with strong dependence onprecipitation, cv = 0.004. Middle panels show cases with an intermediate relationship, cv = 0.003 (see Eqn 2). The upper panels show cases with no effect ofprecipitation on survival in soil (i.e. a uniform survival in soil and cv = 0. Upper panels are identical to the lower panels in Fig. 3 and are shown here forreference.) In all cases Vmax = 0.9.

0 20 400

0.2

0.4

0.6

0.8

1Optimal trait combination

Ger

min

atio

n fr

actio

n

0 20 400

0.2

0.4

0.6

0.8

1

Precipitation standard deviation

See

d m

ass

Vmax = 0.1, cv = 0,

Vmax = 0.5, cv = 0

Vmax = 0.9, cv = 0

Vmax = 0.9, cv = 0.003

Vmax = 0.9, cv = 0.004

Secondary Vmax = 0.5, cv = 0

Secondary Vmax = 0.9, cv = 0

Fig. 6 Summary of the simulation results, showing the optimal trait combinations at different environmental predictability (precipitation standard deviation,x-axis). Solid lines illustrate the optimal germination fraction (G) (left panel) and optimal seed mass (M) (right panel). Each color represents a differentcombination of mean annual survival rate in the soil (Vmax) and relationship between survival in soil and precipitation (cv). Only cases with low meanprecipitation (100mm) are illustrated. At medium and high mean precipitation rates, optimum G andM are the same as in low precipitation with novariation. A secondary co-optimal peak (dashed lines) exists but only at high mean precipitation (280mm), Vmax � 0.5 and cv = 0.





environment when temporal heterogeneity is considered. Theseresults are in contrast with several ESS models that simulate ger-mination rates in spatially homogeneous environments with den-sity dependence (Bulmer, 1984; Ellner, 1985a,b). At the sametime, our results support the hypothesis that some level of seeddormancy is selected for even in temporally constant environ-ments with population density at the equilibrium via a reductionof competition among siblings by spreading their germinationover time (Ellner, 1986). In our model and those of others, suchas the model of Nilsson et al. (1994), density dependence wasintroduced through symmetric competition of a single geneticallyidentical cohort. Therefore, sib-competition could not be distin-guished from generalized intraspecific competition. However,because genetic relatedness was irrelevant in our and Nilssonet al.’s (1994) simulations, generalized competition appears to bea reasonable interpretation of the observed phenomenon.Delayed germination reduces competition among intraspecificcohorts and not exclusively among siblings. Similarly, generalizedcompetition was suggested to be a more realistic natural phenom-enon than sib-completion in several recent theoretical and empir-ical studies (Tielborger & Valleriani, 2005; Lalonde & Roitberg,2006; Satterthwaite, 2010; Eberhart & Tielborger, 2012).

Although we use an overly simplistic representation of the envi-ronment and the phenotypic trait space, our model provides quan-titative predictions about a range of seed mass and germinationfractions optimal under specific environmental conditions, andthe results apply to both intraspecific processes such as evolutionof life history traits, and to inter-specific processes such as commu-nity structure and species coexistence. In particular, we found thatharsh environmental conditions of low precipitation and/orincreased mortality rates in the soil allow only a single optimalcombination of the two traits’ values, thus strongly limiting thepotential number of coexisting species. As the favorability of theenvironment increases, as a function of both an increased amountof precipitation and reduced temporal variation in precipitation,the choice of optimal values for the two-trait combinations

becomes wider. This could potentially allow more species to co-exist, and select for more phenotypic plasticity within species.

The role of differential seed size in promoting species coexis-tence was predicted by several game models (Geritz, 1995; Rees& Westoby, 1997; Geritz et al., 1999), but received no empiricalsupport (Eriksson, 2005). While our model did not directly testmulti-species systems, the simulation results provide furtherdetails about the conditions under which larger and smallerseeded species may coexist. Cases that showed a clear bimodalsolution may indicate not only such natural phenomena as seeddimorphism (i.e. production of both large and small seeds) butalso conditions under which specialization leading to the creationof two distinct co-optimal species is possible. We found that thisstate of multiple co-optimal trait combinations is expected inproductive environments, and in situations in which there iseither a negative relationship between seed mass and survival inthe soil or high survival of seeds in the soil independent of seedmass. Thus, our results indicate that seed survival in the soil canbe important for the coexistence of large and small seed size strat-egies in a given environment.

The results reconcile two alternative explanations for the selec-tive role of seed dormancy and the presence of the soil seed bank,that is, bet-hedging and reduced competition. It is evident fromthe results that both processes took place but under differentenvironmental conditions. Bet-hedging operates and causes adecrease in the germination fraction when environmental favor-ability is low and temporal unpredictability is high, while escapefrom local crowding through dormancy becomes important whenthe environment is favorable and therefore competition is strong.

Acknowledgements

The work was funded in part by grant #10R-05 from theInternational Arid Land Consortium Project to S.V. and G.B.,and NSF grant #DEB-0918869 to G.B. Any opinions, findings,conclusions or recommendations expressed in this material arethose of the authors and do not necessarily reflect the views of theNational Science Foundation. We are grateful to Ashley Mathenyfor editing the manuscript, and Dan Cohen and Benoit Pugol forhelpful comments on an early version of the manuscript.

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Joint evolution of seed traits along an aridity gradient: seed size and dormancy are not two...

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