Gene Regulatory Evolution in Cold-Adapted Fly Populations Neutralizes Plasticity and May Undermine Genetic Canalization.

The relationships between adaptive evolution, phenotypic plasticity, and canalization remain incompletely understood. Theoretical and empirical studies have made conflicting arguments on whether adaptive evolution may enhance or oppose the plastic response. Gene regulatory traits offer excellent potential to study the relationship between plasticity and adaptation, and they can now be studied at the transcriptomic level. Here, we take advantage of three closely related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. We measure the transcriptome-wide plasticity in gene expression levels and alternative splicing (intron usage) between warm and cold laboratory environments. We find that suspected adaptive changes in both gene expression and alternative splicing tend to neutralize the ancestral plastic response. Further, we investigate the hypothesis that adaptive evolution can lead to decanalization of selected gene regulatory traits. We find strong evidence that suspected adaptive gene expression (but not splicing) changes in cold-adapted populations are more vulnerable to the genetic perturbation of inbreeding than putatively neutral changes. We find some evidence that these patterns may reflect a loss of genetic canalization accompanying adaptation, although other processes including hitchhiking recessive deleterious variants may contribute as well. Our findings augment our understanding of genetic and environmental effects on gene regulation in the context of adaptive evolution.

The role of phenotypic plasticity in the establishment of range margins.

It has been argued that adaptive phenotypic plasticity may facilitate range expansions over spatially and temporally variable environments. However, plasticity may induce fitness costs. This may hinder the evolution of plasticity. Earlier modelling studies examined the role of plasticity during range expansions of populations with fixed genetic variance. However, genetic variance evolves in natural populations. This may critically alter model outcomes. We ask: how does the capacity for plasticity in populations with evolving genetic variance alter range margins that populations without the capacity for plasticity are expected to attain? We answered this question using computer simulations and analytical approximations. We found a critical plasticity cost above which the capacity for plasticity has no impact on the expected range of the population. Below the critical cost, by contrast, plasticity facilitates range expansion, extending the range in comparison to that expected for populations without plasticity. We further found that populations may evolve plasticity to buffer temporal environmental fluctuations, but only when the plasticity cost is below the critical cost. Thus, the cost of plasticity is a key factor involved in range expansions of populations with the potential to express plastic response in the adaptive trait. This article is part of the theme issue 'Species' ranges in the face of changing environments (part I)'.

Plasticity, instability and canalization: is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems?

• Evergreen oaks from the Mediterranean basin exhibit a conservative resource-use strategy based on a reduced expression of phenotypic variation (i.e. canalization). We hypothesized that genetic variation across closely related species is more canalized than the response to environmental variation. • Seedlings of Quercus ilex and Q. coccifera, two important oak species from the Mediterranean basin that belong to the same subgenus and section, were grown in contrasted light and nutrient environments following a factorial design. Phenotypic variation was explored in a total of 75 variables including photosynthetic capacity, nutrient allocation, allometric relationships and crown architecture. • Path analysis showed that phenotypic variation was not significantly affected by differences between species but by those between and within environments, which are argued to be primarily linked to phenotypic plasticity and developmental instability, respectively. This finding is interpreted as evidence of genetic canalization across species. • The similar importance of plasticity and instability as sources of phenotypic variation and the high degree of genetic canalization are consistent with the expected role of the environmental unpredictability of Mediterranean ecosystems in shaping the developmental patterns of these two species.