The role of gene regulatory evolution in weapon diversification: Insights from comparative genomics, chromatin profiling, and functional analyses of BMP signaling in horned beetles
- 1Department of Biological Sciences, Mississippi State University, Starkville, Mississippi, United States of America.
- 2Department of Biology, Indiana University, Bloomington, Indiana, United States of America.
Abstract
Condition-responsive growth is a common feature of multicellular development, during which organisms integrate genetic and environmental signals to adjust their phenotype. However, the molecular properties shaping condition-responsive diversification remain poorly understood. The beetle genus Onthophagus offers promising opportunities to investigate this question, given its diversity of sex- and nutrition-responsive phenotypes, including horns — novel, secondary sexual weapons used in reproductive competition. We compared the gene regulatory properties of horns in two closely related species exhibiting highly specialized sex- and nutrition-biased phenotypes. We found a dynamic cis-regulatory landscape in developing horn tissue, shaped by mutational accumulation across species, condition-specific changes in chromatin accessibility within species, and the acquisition of lineage-specific regulatory elements. Many of these putative regulatory regions include binding site motifs of critical developmental regulatory genes, including members of the bone morphogenetic protein signaling pathway. We provide functional evidence that two proteins in this pathway have been co-opted for horn development, influencing the shape and size of this trait across species, sexes, and nutritional states. These findings provide evidence that evolutionarily labile cis-regulatory interactions may evolve alongside diversification of condition-specific traits, potentially modifying the activity of conserved developmental pathways over short evolutionary timescales. Author summary: In this work, we examine a central question in evolutionary biology: how environmental and genetic variation is converted into morphological differences during development. In our study system, Onthophagus horned dung beetles, horn shape and size vary tremendously across species, sexes, and nutritional conditions, making them ideal for studying condition-responsive trait development. We focus on comparing the characteristics of regulatory elements in horn tissue, such as enhancers and promoters, to understand better how gene expression changes during developmental evolution. We show that mutations have accumulated within potentially important developmental regulatory elements across species with divergent horn shapes and nutritional responsiveness. We find that hundreds of elements differ in chromatin accessibility between conditions, including many elements that occur in only a single species. Finally, we find that many candidate regulatory elements harbor binding motifs for key transcription factors, including those involved in bone morphogenetic protein signaling, and we validate that members of this pathway play a complex role in horn development and, potentially, diversification. More broadly, our findings suggest that the evolution of condition-sensitive traits may proceed through relatively rapid changes to regulatory element properties, enabling conserved developmental pathways to generate novel morphologies.
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BibTeX
@article{davidson2026role,
title = {{The role of gene regulatory evolution in weapon diversification: Insights from comparative genomics, chromatin profiling, and functional analyses of BMP signaling in horned beetles}},
author = {Phillip L Davidson and Isabel G Manley and Armin P Moczek},
journal = {PLOS Genetics},
year = {2026},
month = oct,
doi = {10.1371/journal.pgen.1012338},
url = {https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1012338},
note = {CC BY},
}
RIS
TY - JOUR
TI - The role of gene regulatory evolution in weapon diversification: Insights from comparative genomics, chromatin profiling, and functional analyses of BMP signaling in horned beetles
AU - Phillip L Davidson
AU - Isabel G Manley
AU - Armin P Moczek
PY - 2026
DA - 2026/10/21
JO - PLOS Genetics
DO - 10.1371/journal.pgen.1012338
UR - https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1012338
AB - Condition-responsive growth is a common feature of multicellular development, during which organisms integrate genetic and environmental signals to adjust their phenotype. However, the molecular properties shaping condition-responsive diversification remain poorly understood. The beetle genus Onthophagus offers promising opportunities to investigate this question, given its diversity of sex- and nutrition-responsive phenotypes, including horns — novel, secondary sexual weapons used in reproductive competition. We compared the gene regulatory properties of horns in two closely related species exhibiting highly specialized sex- and nutrition-biased phenotypes. We found a dynamic cis-regulatory landscape in developing horn tissue, shaped by mutational accumulation across species, condition-specific changes in chromatin accessibility within species, and the acquisition of lineage-specific regulatory elements. Many of these putative regulatory regions include binding site motifs of critical developmental regulatory genes, including members of the bone morphogenetic protein signaling pathway. We provide functional evidence that two proteins in this pathway have been co-opted for horn development, influencing the shape and size of this trait across species, sexes, and nutritional states. These findings provide evidence that evolutionarily labile cis-regulatory interactions may evolve alongside diversification of condition-specific traits, potentially modifying the activity of conserved developmental pathways over short evolutionary timescales. Author summary: In this work, we examine a central question in evolutionary biology: how environmental and genetic variation is converted into morphological differences during development. In our study system, Onthophagus horned dung beetles, horn shape and size vary tremendously across species, sexes, and nutritional conditions, making them ideal for studying condition-responsive trait development. We focus on comparing the characteristics of regulatory elements in horn tissue, such as enhancers and promoters, to understand better how gene expression changes during developmental evolution. We show that mutations have accumulated within potentially important developmental regulatory elements across species with divergent horn shapes and nutritional responsiveness. We find that hundreds of elements differ in chromatin accessibility between conditions, including many elements that occur in only a single species. Finally, we find that many candidate regulatory elements harbor binding motifs for key transcription factors, including those involved in bone morphogenetic protein signaling, and we validate that members of this pathway play a complex role in horn development and, potentially, diversification. More broadly, our findings suggest that the evolution of condition-sensitive traits may proceed through relatively rapid changes to regulatory element properties, enabling conserved developmental pathways to generate novel morphologies.
SN - 1553-7404
SN - 1553-7390
ER -