Whole-genome resequencing reveals recent divergence of geographic populations of the dung beetle Phelotrupes auratus with color variation

Abstract

Knowledge of population divergence history is key to understanding organism diversification mechanisms. The geotrupid dung beetle Phelotrupes auratus, which inhabits montane forests and exhibits three color forms (red, green, and indigo), diverged into five local populations (west/red, south/green, south/indigo, south/red, and east/red) in the Kinki District of Honshu, Japan, based on the combined interpretation of genetic cluster and color-form data. Here, we estimated the demographic histories of these local populations using the newly assembled draft genome sequence of P. auratus and whole-genome resequencing data obtained from each local population. Using coalescent simulation analysis, we estimated P. auratus population divergences at ca. 3800, 2100, 600, and 200 years ago, with no substantial gene flow between diverged populations, implying the existence of persistent barriers to gene flow. Notably, the last two divergence events led to three local populations with different color forms. The initial divergence may have been affected by climatic cooling around that time, and the last three divergence events may have been associated with the increasing impact of human activities. Both climatic cooling and increasing human activity may have caused habitat fragmentation and a reduction in the numbers of large mammals supplying food (dung) for P. auratus, thereby promoting the decline, segregation, and divergence of local populations. Our research demonstrates that geographic population divergence in an insect with conspicuous differences in traits such as body color may have occurred rapidly under the influence of human activity.