“Ecological genetic conflict: Genetic architecture can shift the balance between local adaptation and plasticity”

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Olof Leimar, Sasha R. X. Dall, John M. McNamara, Bram Kuijper, and Peter Hammerstein (Jan 2019)

The DOI will be https://dx.doi.org/10.1086/700719

Ecological genetic conflict influences local adaptation and phenotypic plasticity

Stronger phenotypic plasticity when genes for plasticity are unlinked to genes for local phenotypic specialization

Ecotype variation in Littorina saxatilis marine snails. In these organisms, different forms are genetically specialized to specific habitats, such as to sheltered boulder shores with high crab predation risk (crab morph, left) or wave-exposed rocky shores (wave morph, right). The shell phenotype is also influenced by environmental conditions during development.
(Credit: Kerstin Johannesson, University of Gothenburg, Sweden)

Many species have phenotypic variants that occur in specific habitats. The sea snails in the illustration are examples of this. The variants are called ecotypes and differ genetically. Often, differing phenotypes are also influenced by local environmental conditions. This is called phenotypic plasticity. In an article appearing in The American Naturalist, Olof Leimar, Sasha Dall, John McNamara, Bram Kuijper, and Peter Hammerstein investigate how important plasticity will be in comparison with genetic local adaptation. The authors are theoretical biologists and use mathematical models to study evolution. They ask whether the position of genes in the genome can influence how strong plasticity and how strong genetic specialization will be. It is known that genes that cause phenotypes to be locally adapted, i.e. suited to a particular habitat, often occur close together in the genome. The authors asked if this is also likely for genes that make an individual plastically sensitive to the local environmental conditions. This question has not been studied before. Surprisingly, the authors found the opposite, that genes evolve more pronounced plasticity if they are unlinked to genes for local adaptation. They hope that this prediction will spur geneticists to investigate the genomics of phenotypic plasticity.


Abstract

Genetic polymorphism can contribute to local adaptation in heterogeneous habitats, for instance as a single locus with alleles adapted to different habitats. Phenotypic plasticity can also contribute to trait variation across habitats, through developmental responses to habitat-specific cues. We show that the genetic architecture of genetically polymorphic and plasticity loci may influence the balance between local adaptation and phenotypic plasticity. These effects of genetic architecture are instances of ecological genetic conflict. A reduced effective migration rate for genes tightly linked to a genetic polymorphism provides an explanation for the effects, and they can occur both for a single trait and for a syndrome of co-adapted traits. Using individual-based simulations and numerical analysis, we investigate how among-habitat genetic polymorphism and phenotypic plasticity depend on genetic architecture. We also study the evolution of genetic architecture itself, in the form of rates of recombination between genetically polymorphic loci and plasticity loci. Our main result is that for plasticity genes that are unlinked to loci with between-habitat genetic polymorphism, the slope of a reaction norm is steeper in comparison with the slope favored by plasticity genes that are tightly linked to genes for local adaptation.