Origin, fate, and architecture of ecologically relevant genetic variation

Abstract

Recent advances in molecular genetics combined with field manipulations are yielding new insight into the origin, evolutionary fate, and genetic architecture of phenotypic variation in natural plant populations, with two surprising implications for the evolution of plant genomes. First, genetic loci exhibiting antagonistic pleiotropy across natural environments appear rare relative to loci that are adaptive in one or more environments and neutral elsewhere. These 'conditionally neutral' alleles should sweep to fixation when they arise, yet genome comparisons find little evidence for such selective sweeps. Second, genes under biotic selection tend to be of larger effect than genes under abiotic selection. Recent theory suggests this may be a consequence of high gene flow among populations under selection for local adaptation.

Figure 1

Local adaptation may be caused by tightly linked genes with reciprocal patterns of conditional neutrality (CN) or antagonistic pleiotropy (AP) at individual loci. (A and B) fitness reaction norms showing (A) genetic tradeoffs, across the entire genome and (B) at an individual locus (antagonistic pleiotropy, AP). (C) Reciprocal patterns of CN in two genetic loci. (D) Linkage disequilibrium between genes in panel C produces a pattern of ‘pseudo-AP’ at linked loci, resulting in a QTL that resembles panel B. Both AP and pseudo-AP with tight linkage disequilibrium can maintain genetic variation in natural populations.

Figure 2

Fitness reaction norms for two alleles at a locus (alleles Q1 in blue and Q2 in red) measured with low (top panel) or high (bottom panel) residual error in benign or harsh environments. Antagonistic pleiotropy is present in both panels but only detected in the top panel where the null hypothesis of equal means can be rejected in both environments.

Figure 3

Hypothetical reaction norms for two alleles at a locus (alleles Q1 in blue and Q2 in red) are modeled as linear or quadratic fitness functions across an environmental gradient (e.g. temperature, moisture or herbivore damage). Reaction norms are drawn such that mean fitness across the environmental gradient is equal between the Q1 and Q2 alleles in each of the four panels, maintaining genetic variation across the gradient. Antagonistic pleiotropy is suggested when alleles are compared only in paired environments marked by A-D or B-D. Conditional neutrality is suggested when alleles are compared only in environments marked A-C, B-C or C-D. When only environments marked A-B are compared, the Q1 allele appears to have higher fitness in all four panels even though alleles have equal fitness when averaged across the gradient.