cis-Regulatory changes in locomotor genes are associated with the evolution of burrowing behavior

Cell Rep. 2022 Feb 15;38(7):110360. doi: 10.1016/j.celrep.2022.110360.

Abstract

How evolution modifies complex, innate behaviors is largely unknown. Divergence in many morphological traits, and some behaviors, is linked to cis-regulatory changes in gene expression. Given this, we compare brain gene expression of two interfertile sister species of Peromyscus mice that show large and heritable differences in burrowing behavior. Species-level differential expression and allele-specific expression in F1 hybrids indicate a preponderance of cis-regulatory divergence, including many genes whose cis-regulation is affected by burrowing behavior. Genes related to locomotor coordination show the strongest signals of lineage-specific selection on burrowing-induced cis-regulatory changes. Furthermore, genetic markers closest to these candidate genes associate with variation in burrow shape in a genetic cross, suggesting an enrichment for loci affecting burrowing behavior near these candidate locomotor genes. Our results provide insight into how cis-regulated gene expression can depend on behavioral context and how this dynamic regulatory divergence between species may contribute to behavioral evolution.

Keywords: Peromyscus; RNA-seq; allele-specific expression; animal behavior; behavioral genetics; burrow; deer mice.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alleles
  • Animals
  • Behavior, Animal / physiology*
  • Evolution, Molecular*
  • Female
  • Gene Expression Regulation*
  • Locomotion / genetics*
  • Male
  • Peromyscus / genetics*
  • Peromyscus / physiology*
  • Phenotype
  • Quantitative Trait Loci / genetics
  • Regulatory Sequences, Nucleic Acid / genetics*