Non-additive effects between genotypes: Implications for competitive fitness assays.

Competitive fitness assays are widely used in evolutionary biology and typically rely on a reference strain to compare different focal genotypes. This approach implicitly relies on the absence of interaction between the competing genotypes. In other words, the performance of the reference strain must not depend on the competitor. This report scrutinized this assumption by competing diverged Drosophila simulans populations against a common reference strain. We detected strong evidence for interaction between the competing genotypes: (1) Frequency-dependent selection was common with opposite effects in genetically diverged populations. (2) Temporal heterogeneity of fitness estimates, which can be partially attributed to a competitor-specific delay in the eclosion of the reference strain. We propose that this inconsistent behavior of the reference strain can be considered a specific case of a genotype × environment interaction. Focal populations could modify the environment of the reference strain, either indirectly by altering the microbiome composition and food availability or directly by genotype-specific cannibalism. Our results provide new insights into the interaction of diverged genotypes and have important implications for the interpretation of competitive fitness assays.

Rapid and biased evolution of canalization during adaptive divergence revealed by dominance in gene expression variability during Arctic charr early development.

Adaptive evolution may be influenced by canalization, the buffering of developmental processes from environmental and genetic perturbations, but how this occurs is poorly understood. Here, we explore how gene expression variability evolves in diverging and hybridizing populations, by focusing on the Arctic charr (Salvelinus alpinus) of Thingvallavatn, a classic case of divergence between feeding habitats. We report distinct profiles of gene expression variance for both coding RNAs and microRNAs between the offspring of two contrasting morphs (benthic/limnetic) and their hybrids reared in common conditions and sampled at two key points of cranial development. Gene expression variance in the hybrids is substantially affected by maternal effects, and many genes show biased expression variance toward the limnetic morph. This suggests that canalization, as inferred by gene expression variance, can rapidly diverge in sympatry through multiple gene pathways, which are associated with dominance patterns possibly biasing evolutionary trajectories and mitigating the effects of hybridization on adaptive evolution.

Temperature-driven gene expression evolution in natural and laboratory populations highlights the crucial role of correlated fitness effects for polygenic adaptation.

The influence of pleiotropy on adaptive responses is a highly controversial topic, with limited empirical evidence available. Recognizing the pivotal role of the correlation of fitness effects, we designed an experiment to compare the adaptive gene expression evolution of natural and experimental populations. To test this, we studied the evolution of gene expression in response to temperature in two Drosophila species on a natural temperature cline in North America and replicated populations evolving in hot- and cold-temperature regimes. If fitness effects of affected traits are independent, pleiotropy is expected to constrain the adaptive response in both settings, laboratory and natural populations. However, when fitness effects are more correlated in natural populations, adaptation in the wild will be facilitated by pleiotropy. Remarkably, we find evidence for both predicted effects. In both settings, genes with strong pleiotropic effects contribute less to adaptation, indicating that the majority of fitness effects are not correlated. In addition, we discovered that genes involved in adaptation exhibited more pleiotropic effects in natural populations. We propose that this pattern can be explained by a stronger correlation of fitness effects in nature. More insights into the dual role of pleiotropy will be crucial for the understanding of polygenic adaptation.