Germination, Postgermination Adaptation, and Species Ecological Ranges

Donohue, Kathleen; Casas, Rafael Rubio de; Burghardt, Liana T.; Kovach, Katherine; Willis, Charles G.

doi:10.1146/annurev-ecolsys-102209-144715

Cited by 777 publications

(865 citation statements)

References 132 publications

(127 reference statements)

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“…One key question is whether local adaptation results from genetic tradeoffs (antagonistic pleiotropy) in which locally favored alleles reduce fitness elsewhere or is caused by alleles that are conditionally neutral (favored in the home environment but selectively neutral in other environments). Empirical studies have rarely detected genetic tradeoffs (12)(13)(14), but these studies typically include only part of the life cycle (3,5,15), possibly resulting in a systematic underestimation of the magnitude of adaptive differentiation and of the occurrence of genetically based tradeoffs.Early life stages can be expected to play a prominent role in local adaptation. First, selection can be particularly severe during the first part of the life cycle when organisms are vulnerable and suffer from high mortality rates (15)(16)(17)(18)(19).…”

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confidence: 99%

“…Empirical studies have rarely detected genetic tradeoffs (12)(13)(14), but these studies typically include only part of the life cycle (3,5,15), possibly resulting in a systematic underestimation of the magnitude of adaptive differentiation and of the occurrence of genetically based tradeoffs.…”

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confidence: 99%

“…Indirect evidence suggests that the seed stage may contribute considerably to local adaptation. Field studies have shown that germination timing is subject to strong natural selection in a wide range of plant species (15,29). In many species, the timing of germination is controlled by seed dormancy, which is a heritable trait (30, 31) that shows evidence of adaptive differentiation.…”

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confidence: 99%

“…First, selection can be particularly severe during the first part of the life cycle when organisms are vulnerable and suffer from high mortality rates (15)(16)(17)(18)(19). Second, conditions early in life often have cascading effects on later life-history traits (16,20,21).…”

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Early life stages contribute strongly to local adaptation in Arabidopsis thaliana

Postma

Ågren

2016

Proc. Natl. Acad. Sci. U.S.A.

122

171

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The magnitude and genetic basis of local adaptation is of fundamental interest in evolutionary biology. However, field experiments usually do not consider early life stages, and therefore may underestimate local adaptation and miss genetically based tradeoffs. We examined the contribution of differences in seedling establishment to adaptive differentiation and the genetic architecture of local adaptation using recombinant inbred lines (RIL) derived from a cross between two locally adapted populations (Italy and Sweden) of the annual plant Arabidopsis thaliana. We planted freshly matured, dormant seeds (>180 000) representing >200 RILs at the native field sites of the parental genotypes, estimated the strength of selection during different life stages, mapped quantitative trait loci (QTL) for fitness and its components, and quantified selection on seed dormancy. We found that selection during the seedling establishment phase contributed strongly to the fitness advantage of the local genotype at both sites. With one exception, local alleles of the eight distinct establishment QTL were favored. The major QTL for establishment and total fitness showed evidence of a fitness tradeoff and was located in the same region as the major seed dormancy QTL and the dormancy gene DELAY OF GERMINATION 1 (DOG1). RIL seed dormancy could explain variation in seedling establishment and fitness across the life cycle. Our results demonstrate that genetically based differences in traits affecting performance during early life stages can contribute strongly to adaptive differentiation and genetic tradeoffs, and should be considered for a full understanding of the ecology and genetics of local adaptation.I dentifying the ecological and genetic mechanisms underlying local adaptation, defined as the local genotype outperforming nonlocal genotypes (1), is a central problem in evolutionary biology. Local adaptation is common in both plant and animal species (2-5), promotes the maintenance of genetic variation (6, 7), and is a key component of models of speciation (8, 9). However, the relative importance of traits contributing to adaptive differentiation and their underlying genetic architecture remain poorly known (1,7,10,11). One key question is whether local adaptation results from genetic tradeoffs (antagonistic pleiotropy) in which locally favored alleles reduce fitness elsewhere or is caused by alleles that are conditionally neutral (favored in the home environment but selectively neutral in other environments). Empirical studies have rarely detected genetic tradeoffs (12)(13)(14), but these studies typically include only part of the life cycle (3,5,15), possibly resulting in a systematic underestimation of the magnitude of adaptive differentiation and of the occurrence of genetically based tradeoffs.Early life stages can be expected to play a prominent role in local adaptation. First, selection can be particularly severe during the first part of the life cycle when organisms are vulnerable and suffer from high mortality rates (15)(16)(...

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confidence: 99%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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Early life stages contribute strongly to local adaptation in Arabidopsis thaliana

Postma

Ågren

2016

Proc. Natl. Acad. Sci. U.S.A.

122

171

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“…Seed dormancy mechanisms are intrinsic blocks to the completion of germination during (temporary) favorable environmental conditions (Finch-Savage and Leubner-Metzger, 2006;Alonso-Blanco et al, 2009;Donohue et al, 2010). These blocks to germination have evolved differently across species through adaptation to the prevailing environment, so that germination occurs when conditions for establishing a new plant generation are likely to be suitable.…”

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Spatiotemporal Seed Development Analysis Provides Insight into Primary Dormancy Induction and Evolution of theLepidium DELAY OF GERMINATION1Genes

et al. 2013

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Seed dormancy is a block to the completion of germination of an intact viable seed under favorable conditions and is an adaptive and agronomically important trait. Thus, elucidating conserved features of dormancy mechanisms is of great interest. The worldwide-distributed genus Lepidium (Brassicaceae) is well suited for cross-species comparisons investigating the origin of common or specific early-life-history traits. We show here that homologs of the seed dormancy-specific gene DELAY OF GERMINATION1 (DOG1) from Arabidopsis (Arabidopsis thaliana) are widespread in the genus Lepidium. The highly dormant Lepidium papillosum is a polyploid species and possesses multiple structurally diversified DOG1 genes (LepaDOG1), some being expressed in seeds. We used the largely elongated and well-structured infructescence of L. papillosum for studying primary dormancy induction during seed development and maturation with high temporal resolution. Using simultaneous germination assays and marker protein expression detection, we show that LepaDOG1 proteins are expressed in seeds during maturation prior to dormancy induction. Accumulation of LepaDOG1 takes place in seeds that gain premature germinability before and during the seed-filling stage and declines during the late maturation and desiccation phase when dormancy is induced. These analyses of the Lepidium DOG1 genes and their protein expression patterns highlight similarities and species-specific differences of primary dormancy induction mechanism(s) in the Brassicaceae.

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Facilitation and competition interact with seed dormancy to affect population dynamics in annual plants

Leverett

Shaw

2019

Population Ecology

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Seed dormancy increases population size via bet‐hedging and by limiting negative interactions (e.g., competition) among individuals. On the other hand, individuals also interact positively (e.g., facilitation), and in some systems, facilitation among juveniles precedes competition among adults in the same generation. Nevertheless, studies of the benefits of seed dormancy typically ignore facilitation. Using a population growth model, we ask how the facilitation–competition balance interacts with seed dormancy rate to affect population dynamics in constant and variable environments. Facilitation increases the growth rate and equilibrium size (in both constant and variable environments) and reduces the extinction rate of populations (in a variable environment), and a higher rate of seed dormancy allows populations with facilitation to reach larger sizes. However, the combined benefits of facilitation and a high dormancy rate only occur in large populations. In small populations, weak facilitation does not affect the growth rate, but does induce a weak demographic Allee effect (where population growth decreases with decreasing population size). Our results suggest that facilitation within populations can interact with bet‐hedging traits (such as dormancy) or other traits that mediate density to affect population dynamics. Further, by ensuring survival but limiting reproduction, ontogenetic switches from facilitation to competition may enable populations to persist but limit their maximum size in variable environments. Such intrinsic regulation of populations could then contribute to the maintenance of similar species within communities.

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Germination, Postgermination Adaptation, and Species Ecological Ranges

Cited by 777 publications

References 132 publications

Early life stages contribute strongly to local adaptation in Arabidopsis thaliana

Early life stages contribute strongly to local adaptation in Arabidopsis thaliana

Spatiotemporal Seed Development Analysis Provides Insight into Primary Dormancy Induction and Evolution of theLepidium DELAY OF GERMINATION1Genes

Facilitation and competition interact with seed dormancy to affect population dynamics in annual plants

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