PT  - JOURNAL ARTICLE
AU  - Lewis, James J.
AU  - Van Belleghem, Steven M.
AU  - Papa, Riccardo
AU  - Danko, Charles G.
AU  - Reed, Robert D.
TI  - Many functionally connected loci foster adaptive diversification along a neotropical hybrid zone
AID  - 10.1126/sciadv.abb8617
DP  - 2020 Sep 01
TA  - Science Advances
PG  - eabb8617
VI  - 6
IP  - 39
4099  - http://advances.sciencemag.org/content/6/39/eabb8617.short
4100  - http://advances.sciencemag.org/content/6/39/eabb8617.full
SO  - Sci Adv2020 Sep 01; 6
AB  - Characterizing the genetic complexity of adaptation and trait evolution is a major emphasis of evolutionary biology and genetics. Incongruent findings from genetic studies have resulted in conceptual models ranging from a few large-effect loci to massively polygenic architectures. Here, we combine chromatin immunoprecipitation sequencing, Hi-C, RNA sequencing, and 40 whole-genome sequences from Heliconius butterflies to show that red color pattern diversification occurred via many genomic loci. We find that the red wing pattern master regulatory transcription factor Optix binds dozens of loci also under selection, which frequently form three-dimensional adaptive hubs with selection acting on multiple physically interacting genes. Many Optix-bound genes under selection are tied to pigmentation and wing development, and these loci collectively maintain separation between adaptive red color pattern phenotypes in natural populations. We propose a model of trait evolution where functional connections between loci may resolve much of the disparity between large-effect and polygenic evolutionary models.