The Genetic Architecture of Parallel Armor Plate Reduction in Threespine Sticklebacks

Department of Developmental Biology and Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, California, USA.
PLoS Biology (Impact Factor: 9.34). 06/2004; 2(5):E109. DOI: 10.1371/journal.pbio.0020109
Source: PubMed

ABSTRACT How many genetic changes control the evolution of new traits in natural populations? Are the same genetic changes seen in cases of parallel evolution? Despite long-standing interest in these questions, they have been difficult to address, particularly in vertebrates. We have analyzed the genetic basis of natural variation in three different aspects of the skeletal armor of threespine sticklebacks (Gasterosteus aculeatus): the pattern, number, and size of the bony lateral plates. A few chromosomal regions can account for variation in all three aspects of the lateral plates, with one major locus contributing to most of the variation in lateral plate pattern and number. Genetic mapping and allelic complementation experiments show that the same major locus is responsible for the parallel evolution of armor plate reduction in two widely separated populations. These results suggest that a small number of genetic changes can produce major skeletal alterations in natural populations and that the same major locus is used repeatedly when similar traits evolve in different locations.

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Available from: Dolph Schluter, Sep 27, 2015
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    • "Linked chromosome 4 and 20 alleles promoting reduction of gill raker length (this study) and gill raker number (Glazer et al. 2014; Miller et al. 2014) might promote co-evolution of these phenotypes in freshwater environments. In sticklebacks, a predictable, shared genetic basis has been found to underlie the convergent evolution of several evolved phenotypes (Chan et al. 2010; Colosimo et al. 2004, 2005; Glazer et al. 2014; Miller et al. 2007). In contrast to these studies, we detected no overlapping gill raker length QTL in the two crosses. "
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    ABSTRACT: Marine populations of the threespine stickleback (Gasterosteus aculeatus) have repeatedly colonized and rapidly adapted to freshwater habitats, providing a powerful system to map the genetic architecture of evolved traits. Here we developed and applied a binned Genotyping-by-Sequencing (GBS) method to build dense genome-wide linkage maps of sticklebacks, using two large marine by freshwater F2 crosses of over 350 fish each. The resulting linkage maps significantly improve the genome assembly by anchoring 78 new scaffolds to chromosomes, reorienting 40 scaffolds, and rearranging scaffolds in 4 locations. In the revised genome assembly, 94.6% of the assembly was anchored to a chromosome. To assess linkage map quality, we mapped quantitative trait loci (QTL) controlling lateral plate number, which mapped as expected to a 200 kilobase genomic region containing Ectodysplasin, as well as a chromosome 7 QTL overlapping a previously identified modifier QTL. Finally, we mapped eight QTL controlling convergently evolved reductions in gill raker length in the two crosses, which revealed that this classic adaptive trait has a surprisingly modular and non-parallel genetic basis. Copyright © 2015 Author et al.
    G3-Genes Genomes Genetics 06/2015; 5(7). DOI:10.1534/g3.115.017905 · 3.20 Impact Factor
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    • "Surprisingly, evolvability has rarely been considered conceptually in populations showing rapid intraspecific ecological divergence into different ecomorphs. Instead research has usually focused on determining the genetic basis of putatively adaptive traits (e.g., Colosimo et al. 2004; Rogers et al. 2007; Albert et al. 2008; Chan et al. 2010). Many of these studies have taken a quantitative trait locus (QTL) approach whereby backcross or F2 hybrids between different ecomorphs are created and reared in common garden experiments. "
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    ABSTRACT: The genetic variance that determines phenotypic variation can change across environments through developmental plasticity and in turn play a strong role in evolution. Induced changes in genotype-phenotype relationships should strongly influence adaptation by exposing different sets of heritable variation to selection under some conditions, while also hiding variation. Therefore, the heritable variation exposed or hidden from selection is likely to differ among habitats. We used ecomorphs from two divergent populations of Arctic charr (Salvelinus alpinus) to test the prediction that genotype-phenotype relationships would change in relation to environment. If present over several generations this should lead to divergence in genotype-phenotype relationships under common conditions, and to changes in the amount and type of hidden genetic variance that can evolve. We performed a common garden experiment whereby two ecomorphs from each of two Icelandic lakes were reared under conditions that mimicked benthic and limnetic prey to induce responses in craniofacial traits. Using microsatellite based genetic maps, we subsequently detected QTL related to these craniofacial traits. We found substantial changes in the number and type of QTL between diet treatments and evidence that novel diet treatments can in some cases provide a higher number of QTL. These findings suggest that selection on phenotypic variation, which is both genetically and environmentally determined, has shaped the genetic architecture of adaptive divergence in Arctic charr. However, while adaptive changes are occurring in the genome there also appears to be an accumulation of hidden genetic variation for loci not expressed in the contemporary environment.
    Evolution & Development 06/2014; 16(4). DOI:10.1111/ede.12087 · 2.72 Impact Factor
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    • "The freshwater individuals were significantly more active than marine fish, although they did not differ in boldness. This is in line with the hypothesis that the freshwater behaviour stems from standing genetic variation in the marine population, as very bold individuals could also be found in the marine population, as observed in previous studies for morphological traits in threespine stickleback [50]. In this case, natural selection acting on these individuals once in the new freshwater environment is also possible. "
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    ABSTRACT: Colonisation of novel environments means facing new ecological challenges often resulting in the evolution of striking divergence in phenotypes. However, little is known about behavioural divergence following colonisation, despite the predicted importance of the role of behavioural phenotype-environment associations in adaptive divergence. We studied the threespine stickleback (Gasterosteus aculeatus), a model system for postglacial colonisation of freshwater habitats largely differing in ecological conditions from the ones faced by the descendants of the marine ancestor. We found that common-environment reared freshwater juveniles were less social, more active and more aggressive than their marine counterparts. This behavioural divergence could represent the result of natural selection that acted on individuals following freshwater colonisation, with predation as a key selection agent. Alternatively, the behavioural profile of freshwater juveniles could represent the characteristics of individuals that preferentially invaded freshwater after the glacial retreat, drawn from the standing variation present in the marine population.
    PLoS ONE 06/2014; 9(6):e98980. DOI:10.1371/journal.pone.0098980 · 3.23 Impact Factor
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