A pleiotropic hitchhiking model recapitulates alignments between fly wing divergence and variation

Abstract

The alignment among mutational variance (M), standing genetic variance (G), and macroevolutionary divergence (R) in Drosophila wing shape poses a rate paradox under a simple constraint hypothesis: evolution follows mutational lines of least resistance, yet proceeds orders of magnitude slower than the abundant genetic variation would permit. This is difficult to reconcile with a simple constraint view in which long-term evolution merely tracks the amount of available variation in each direction. Previous explanations invoke deleterious pleiotropy on unmeasured traits or correlational selection on trait combinations, but recent empirical work finds little evidence of fitness costs beyond flight performance. Here, by reanalyzing published data, I show that wing size shows the hallmark of the primary selection target: among all wing traits, size exhibits the lowest ratio of standing genetic to mutational variance, indicating the strongest selective depletion. Based on this empirical observation, I develop a single-axis selection model in which natural selection targets only a single trait while all other traits evolve as correlated byproducts via within-module pleiotropy. This minimal model reproduces both the observed M -G-R alignment and slower-than-neutral divergence rates, explaining micro- and macroevolutionary patterns in fly wings without invoking complex adaptive landscapes. Significance StatementA fundamental question in biology is whether large-scale evolutionary patterns arise from the same processes that drive change within populations. Fly wing shape offers a striking test case: the directions of genetic variation and species divergence are closely aligned, yet wing shape evolves far more slowly than expected -- a rate paradox under a simple constraint hypothesis. I show that this paradox can be explained by a simple mechanism: natural selection on one trait indirectly constrains the evolution of other non-selected traits through within-module pleiotropy. This single-axis selection model reproduces observed evolutionary patterns without requiring complex multivariate selection, and its prediction that wing size is the primary target of selection is supported by reanalysis of published data. The framework applies broadly to any trait that shares mutations with correlated characters.