Evolution in parallel: new insights from a classic system

Foster, Susan A.

doi:10.1016/j.tree.2004.07.004

Cited by 51 publications

(42 citation statements)

References 26 publications

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“…Developmental recombination offers an alternative explanation for parallelism in stickleback (5,30). The recurrence of this pair of forms suggests that there may be something about the development of their common ancestor that enables it to give rise to these two particular forms readily, by means of altered expression of ancestral traits.…”

Section: Developmental Recombination and Parallel Species Pairsmentioning

confidence: 99%

Developmental plasticity and the origin of species differences

West‐Eberhard

2005

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

810

661

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Speciation is the origin of reproductive isolation and divergence between populations, according to the ''biological species concept'' of Mayr. Studies of reproductive isolation have dominated research on speciation, leaving the origin of species differences relatively poorly understood. Here, I argue that the origin of species differences, and of novel phenotypes in general, involves the reorganization of ancestral phenotypes (developmental recombination) followed by the genetic accommodation of change. Because selection acts on phenotypes, not directly on genotypes or genes, novel traits can originate by environmental induction as well as mutation, then undergo selection and genetic accommodation fueled by standing genetic variation or by subsequent mutation and genetic recombination. Insofar as phenotypic novelties arise from adaptive developmental plasticity, they are not ''random'' variants, because their initial form reflects adaptive responses with an evolutionary history, even though they are initiated by mutations or novel environmental factors that are random with respect to (future) adaptation. Change in trait frequency involves genetic accommodation of the threshold or liability for expression of a novel trait, a process that follows rather than directs phenotypic change. Contrary to common belief, environmentally initiated novelties may have greater evolutionary potential than mutationally induced ones. Thus, genes are probably more often followers than leaders in evolutionary change. Species differences can originate before reproductive isolation and contribute to the process of speciation itself. Therefore, the genetics of speciation can profit from studies of changes in gene expression as well as changes in gene frequency and genetic isolation.speciation ͉ genetic accommodation ͉ adaptive evolution ͉ novelty ͉ parallel evolution

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Section: Developmental Recombination and Parallel Species Pairsmentioning

confidence: 99%

Developmental plasticity and the origin of species differences

West‐Eberhard

2005

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

810

661

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“…These speciation events in stickleback correspond to significant environmental differences, such as salinity and temperature variation between ocean and freshwater habitats, or benthic and limnetic niches in fresh water [63,[66][67][68][69][70][71][72][73][74][75]. Research has progressed rapidly in defining the genetic basis of some evolving traits in freshwater stickleback [62,[76][77][78], including variation in armour, coloration and craniofacial attributes, among others [79][80][81][82][83][84]. In laboratory crosses, genetic variation in these traits has been attributed to a relatively small number of genomic regions [80,81,[84][85][86][87][88][89].…”

Section: Introductionmentioning

confidence: 99%

Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes

Hohenlohe

Bassham

Currey

et al. 2012

Phil. Trans. R. Soc. B

201

226

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Population genomic studies are beginning to provide a more comprehensive view of dynamic genomescale processes in evolution. Patterns of genomic architecture, such as genomic islands of increased divergence, may be important for adaptive population differentiation and speciation. We used nextgeneration sequencing data to examine the patterns of local and long-distance linkage disequilibrium (LD) across oceanic and freshwater populations of threespine stickleback, a useful model for studies of evolution and speciation. We looked for associations between LD and signatures of divergent selection, and assessed the role of recombination rate variation in generating LD patterns. As predicted under the traditional biogeographic model of unidirectional gene flow from ancestral oceanic to derived freshwater stickleback populations, we found extensive local and long-distance LD in fresh water. Surprisingly, oceanic populations showed similar patterns of elevated LD, notably between large genomic regions previously implicated in adaptation to fresh water. These results support an alternative biogeographic model for the stickleback radiation, one of a metapopulation with appreciable bidirectional gene flow combined with strong divergent selection between oceanic and freshwater populations. As predicted by theory, these processes can maintain LD within and among genomic islands of divergence. These findings suggest that the genomic architecture in oceanic stickleback populations may provide a mechanism for the rapid re-assembly and evolution of multi-locus genotypes in newly colonized freshwater habitats, and may help explain genetic mapping of parallel phenotypic variation to similar loci across independent freshwater populations.

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“…Reduced competition and distinct niches have created conditions where directional selection has led to speciation, particularly in temperate northern lakes (Robinson and Schluter 2000;Landry et al 2007). A forward genetic approach (from phenotype to genotype) has been used in these systems to elucidate the genetic basis of adaptive phenotypes (e.g., Foster and Baker 2004). Under this approach, QTL studies have been used to understand the genetic architecture of adaptive traits by examining the number, magnitude, and direction of underlying loci (Peichel et al 2001;.…”

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confidence: 99%

The Phenomics and Expression Quantitative Trait Locus Mapping of Brain Transcriptomes Regulating Adaptive Divergence in Lake Whitefish Species Pairs (Coregonus sp.)

Whiteley

Derôme

Rogers³

et al. 2008

Genetics

107

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We used microarrays and a previously established linkage map to localize the genetic determinants of brain gene expression for a backcross family of lake whitefish species pairs (Coregonus sp.). Our goals were to elucidate the genomic distribution and sex specificity of brain expression QTL (eQTL) and to determine the extent to which genes controlling transcriptional variation may underlie adaptive divergence in the recently evolved dwarf (limnetic) and normal (benthic) whitefish. We observed a sex bias in transcriptional genetic architecture, with more eQTL observed in males, as well as divergence in genome location of eQTL between the sexes. Hotspots of nonrandom aggregations of up to 32 eQTL in one location were observed. We identified candidate genes for species pair divergence involved with energetic metabolism, protein synthesis, and neural development on the basis of colocalization of eQTL for these genes with eight previously identified adaptive phenotypic QTL and four previously identified outlier loci from a genome scan in natural populations. Eighty-eight percent of eQTL-phenotypic QTL colocalization involved growth rate and condition factor QTL, two traits central to adaptive divergence between whitefish species pairs. Hotspots colocalized with phenotypic QTL in several cases, revealing possible locations where master regulatory genes, such as a zinc-finger protein in one case, control gene expression directly related to adaptive phenotypic divergence. We observed little evidence of colocalization of brain eQTL with behavioral QTL, which provides insight into the genes identified by behavioral QTL studies. These results extend to the transcriptome level previous work illustrating that selection has shaped recent parallel divergence between dwarf and normal lake whitefish species pairs and that metabolic, more than morphological, differences appear to play a key role in this divergence.

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Evolution in parallel: new insights from a classic system

Cited by 51 publications

References 26 publications

Developmental plasticity and the origin of species differences

Developmental plasticity and the origin of species differences

Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes

The Phenomics and Expression Quantitative Trait Locus Mapping of Brain Transcriptomes Regulating Adaptive Divergence in Lake Whitefish Species Pairs (Coregonus sp.)

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