Early life stages contribute strongly to local adaptation in Arabidopsis thaliana

Abstract

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)(...

Multiple alleles at a single locus control seed dormancy in Swedish Arabidopsis

“…Of course there will be further mortality in the seed bank and not all established seedlings will survive and reproduce, but the results serve to illustrate that selection on DOG1 could be very strong indeed, and lend credence to the notion that the observed distribution of dormancy and DOG1 alleles (Figures 1C and 3D) reflects local adaptation. Although our experiments have limitations and do not allow us to decompose total fitness, our results agree with those from previous studies, and it becomes very clear that germination timing is one of the main (if not the main) fitness components (Postma and Ågren, 2016; Huang et al, 2010a). To fully understand how selection acts will require multi-generational field experiments as selection pressures are likely to vary from year to year (and are unlikely to be at equilibrium, because of large-scale climate variations).…”

“…As a consequence, we could only estimate survival between dispersal in June and the onset of winter in November. Postma et al (2016) have shown that survival during this phase is critical to plant performance. Thus, we believe that our estimations of ‘fitness’ are realistic.…”

“…The DOG1 locus harbors a series of functionally distinct alleles segregating in wild populations, and exhibits a pattern of genetic differentiation suggestive of local adaptation (Kronholm et al, 2012). Moreover, field experiments using a diallel cross between accessions from Sweden and Italy identified a major QTL associated with total fitness that spanned the DOG1 region, and also demonstrated that genetic differences in seedling establishment—and most particularly in seed dormancy—are one of the main components of local adaptation (Postma and Ågren, 2016; Postma et al, 2016; Huang et al, 2010a). Finally, extensive natural variation for seed dormancy is not unique to the DOG1 locus and many other QTLs have been mapped in various populations (Alonso-Blanco et al, 2003; Bentsink et al, 2006, 2010; Amiguet-Vercher et al, 2015; Xiang et al, 2016).…”

“…For a weedy annual like Arabidopsis thaliana , the subject of our study, germinating at the right time is crucial for early survival, and also influences other life history traits, such as flowering (Postma and Ågren, 2016; Huang et al, 2010a; Chiang et al, 2013; Donohue et al, 2010; Springthorpe and Penfield, 2015). Seed dormancy varies geographically, with high dormancy being associated with long, dry summers, and low dormancy being more prevalent where summers are short and wet (Chiang et al, 2011; Debieu et al, 2013; Kronholm et al, 2012).…”

Phenotypic plasticity and local adaptation favor range expansion of a Neotropical palm

“…Reciprocal transplants have predominantly been applied for herbaceous and shrubby species growing in temperate regions (Fenster & Galloway, 2000; Franks, Weber, & Aitken, 2014; Grassein, Lavorel, & Till‐Bottraud, 2014; Malikova, Latzel, Smilauer, & Klimesova, 2016), with few exceptions in the tropics (Chen & Schemske, 2015), because it may take several years to evaluate the overall plant performance during an individual's life span. Although all the phases should be studied in order to obtain the complete picture of ecotypic adaptations, in arboreal species it may be methodologically appropriate, if not plainly inevitable, to split the cycle into practical sets of phases: As Darwin 1994, page 86, put it: “… so in a state of nature, natural selection will be enabled to act on and modify organic beings at any age, by the accumulation of profitable variations at that age, and by their inheritance at a corresponding age.” As significant plant mortality occurs during the seedling establishment and sapling growth phenophases, natural selection should in theory strongly benefit variants within plant populations with higher plant performance in these phases (Postma & Agren, 2016). Hence, plant performance during seedling establishment and sapling initial growth of long‐lived species should logically be a reliable indicator of ecotypic differentiation in the context of range size and habitat distribution.…”