Local Adaptation, Phenotypic Differentiation, and Hybrid Fitness in Diverged Natural Populations of Arabidopsis Lyrata

Leinonen, Päivi H.; Remington, David L.; Savolainen, Outi

doi:10.1111/j.1558-5646.2010.01119.x

Cited by 69 publications

(100 citation statements)

References 78 publications

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“…Additional F 2 plants from this cross were grown in their native habitats (Norway and North Carolina). In North Carolina, hybrid fitness was intermediate to the parental populations but in Norway the F 2 hybrids surprisingly showed heterosis (Leinonen et al 2011). Thus, the observed TRD in F 2 would not be expected to be due to low seed germination success or high mortality in later life stages.…”

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confidence: 93%

Investigating Incipient Speciation in Arabidopsis lyrata from Patterns of Transmission Ratio Distortion

2013

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Our understanding of the development of intrinsic reproductive isolation is still largely based on theoretical models and thorough empirical studies on a small number of species. Theory suggests that reproductive isolation develops through accumulation of epistatic genic incompatibilities, also known as Bateson-Dobzhansky-Muller (BDM) incompatibilities. We can detect these from marker transmission ratio distortion (TRD) in hybrid progenies of crosses between species or populations, where TRD is expected to result from selection against heterospecific allele combinations in hybrids. TRD may also manifest itself because of intragenomic conflicts or competition between gametes or zygotes. We studied early stage speciation in Arabidopsis lyrata by investigating patterns of TRD across the genome in F 2 progenies of three reciprocal crosses between four natural populations. We found that the degree of TRD increases with genetic distance between crossed populations, but also that reciprocal progenies may differ substantially in their degree of TRD. Chromosomes AL6 and especially AL1 appear to be involved in many single-and two-locus distortions, but the location and source of TRD vary between crosses and between reciprocal progenies. We also found that the majority of single-and two-locus TRD appears to have a gametic, as opposed to zygotic, origin. Thus, while theory on BDM incompatibilities is typically illustrated with derived nuclear alleles proving incompatible in hybrid zygotes, our results suggest a prominent role for distortions emerging before zygote formation. C OMPLETE reproductive isolation between natural populations is usually achieved through several reproductive barriers, acting at different developmental stages. In plants prezygotic reproductive isolation acts either prepollination (e.g., habitat, temporal, or pollinator isolation) or postpollination (e.g., unilateral incompatibility or conspecific pollen precedence). Postzygotic isolating mechanisms either reduce viability, fertility, or fitness of hybrids or prevent development of a hybrid altogether. The effect of postzygotic reproductive barriers may be environment dependent (e.g., Hatfield and Schluter 1999) or independent of the environment. The latter, intrinsic postzygotic barriers, cause reduced viability or fertility of hybrids and have been studied extensively, e.g., in Drosophila (for a review see Coyne and Orr 2004;Presgraves 2010).Despite the importance of development of reproductive isolation as an evolutionary process, and despite considerable study, precise molecular genetic mechanisms of postzygotic isolation have rarely been described (Presgraves 2010;Rieseberg and Blackman 2010). It is generally assumed, however, that intrinsic postzygotic isolation is due to Bateson-Dobzhansky-Muller incompatibilities (BDMI;Orr 1995;Orr and Turelli 2001). These incompatibilities emerge when in (usually) isolated populations new alleles arise, which upon secondary contact do not function together. In a few cases single genes involved in BD...

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confidence: 93%

Investigating Incipient Speciation in Arabidopsis lyrata from Patterns of Transmission Ratio Distortion

2013

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“…Seedlings were initially grown in a greenhouse in Lom, Norway, and field planting was done in June 2005 at a closer 10 3 10 cm spacing due to the much slower growth of plants in the Norway environment. A total of 479 F 2 plants were planted in Norway from the same crosses used for the North Carolina planting, as described previously (Leinonen et al 2011(Leinonen et al , 2013. As in North Carolina, these plants were evenly divided across eight blocks along with plants from full-sib families from Spiterstulen, Mayodan, and two other populations, and were located randomly within blocks.…”

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Complex Genetic Effects on Early Vegetative Development Shape Resource Allocation Differences BetweenArabidopsis lyrataPopulations

et al. 2013

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Costs of reproduction due to resource allocation trade-offs have long been recognized as key forces in life history evolution, but little is known about their functional or genetic basis. Arabidopsis lyrata, a perennial relative of the annual model plant A. thaliana with a wide climatic distribution, has populations that are strongly diverged in resource allocation. In this study, we evaluated the genetic and functional basis for variation in resource allocation in a reciprocal transplant experiment, using four A. lyrata populations and F 2 progeny from a cross between North Carolina (NC) and Norway parents, which had the most divergent resource allocation patterns. Local alleles at quantitative trait loci (QTL) at a North Carolina field site increased reproductive output while reducing vegetative growth. These QTL had little overlap with flowering date QTL. Structural equation models incorporating QTL genotypes and traits indicated that resource allocation differences result primarily from QTL effects on early vegetative growth patterns, with cascading effects on later vegetative and reproductive development. At a Norway field site, North Carolina alleles at some of the same QTL regions reduced survival and reproductive output components, but these effects were not associated with resource allocation trade-offs in the Norway environment. Our results indicate that resource allocation in perennial plants may involve important adaptive mechanisms largely independent of flowering time. Moreover, the contributions of resource allocation QTL to local adaptation appear to result from their effects on developmental timing and its interaction with environmental constraints, and not from simple models of reproductive costs. DIFFERENTIAL allocation of resources to current reproduction vs. continued growth and maintenance is a central feature of life history differences among organisms (Stearns 1992;Roff and Fairbairn 2007). Reproduction is widely recognized as costly, leading to trade-offs between investment in reproduction vs. growth and maintenance and ultimately survival (Bell 1980;Reznick 1985;Lovett Doust 1989). Optimal resource allocation strategies are likely to vary by environment due to differential effects of allocation on growth rates, survival, and fecundity, thus leading to selection for different allocation strategies in different environments (Williams 1966;Charnov and Schaffer 1973;Bell 1980;Reznick 1985;Biere 1995;Johnson 2007).Among iteroparous organisms, which must allocate some resources to somatic maintenance in order to survive to reproduce multiple times, a wide range of proportional investments in growth and maintenance vs. reproduction is possible (van Noordwijk and De Jong 1986). Genetic variation in traits subject to trade-offs results in what has been termed "structured pleiotropy," in which genetic covariances between traits result from functional constraints imposed by the limiting resources (De Jong 1990;Stearns et al. 1991; see Figure 1B). However, differences in resource acquisi...

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“…19,20 More recently, local adaptation of cytoplasm was observed in a comparison of American and European populations of Arabidopsis lyrata, a relative of the model species A. thaliana. 10 These observations indicate that intraspecific variation in the cytoplasm can contribute to adaptive population differentiation.…”

Section: Arabidopsis Thaliana As a Model To Investigate The Cytoplasmmentioning

confidence: 95%

“…A number of studies that have detected a cytoplasmic effect on fitness or local adaptation also show significant cytoplasm x nuclear genotype interactions. 10,[17][18][19] A recent report on the Rubisco large subunit shows that its evolution has been shaped by the combined effect of adaptation and the structural and biochemical constraints that result, at least in part, from functional interactions with nuclear encoded proteins. 27 Therefore, the study of "cytoplasmic adaptation" also implies identifying nuclear encoded factors whose variation is coupled with that of cytoplasmic genes as a result of co-adaptation.…”

Section: Scientific Questionsmentioning

confidence: 99%

“…4 In these aspects, model species, such as Arabidopsis thaliana and its relatives, contribute significantly to the development of highly efficient methods for identifying genes underlying ecologically relevant traits, such as traditional linkage mapping and, more recently, genome-wide association mapping. [5][6][7][8][9][10] Most-not to say all-of the above-mentioned studies focus on variation in nuclear genes and very few genetic studies consider the contribution of organelle genomes to adaptation. Nevertheless, a number of reports in various scientific fields provide converging evidence that variations in organelle genomes *Correspondence to: Françoise Budar; Email: Francoise.Budar@versailles.inra.fr Submitted: 01/28/11; Accepted: 01/28/11 DOI: 10.4161/psb.…”

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The role of organelle genomes in plant adaptation

Budar

Roux

2011

Plant Signaling & Behavior

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Local Adaptation, Phenotypic Differentiation, and Hybrid Fitness in Diverged Natural Populations of Arabidopsis Lyrata

Cited by 69 publications

References 78 publications

Investigating Incipient Speciation in Arabidopsis lyrata from Patterns of Transmission Ratio Distortion

Investigating Incipient Speciation in Arabidopsis lyrata from Patterns of Transmission Ratio Distortion

Complex Genetic Effects on Early Vegetative Development Shape Resource Allocation Differences BetweenArabidopsis lyrataPopulations

The role of organelle genomes in plant adaptation

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