Exploitation of an ancestral pheromone biosynthetic pathway contributes to diversification in Heliconius butterflies

TY - JOUR

T1 - Exploitation of an ancestral pheromone biosynthetic pathway contributes to diversification in Heliconius butterflies

AU - Cama, Bruna

AU - Ehlers, Stephanie

AU - Szczerbowski, Daiane

AU - Thomas-Oates, Jane

AU - Jiggins, Chris D.

AU - Schulz, Stefan

AU - McMillan, W. Owen

AU - Dasmahapatra, Kanchon K.

N1 - © 2022 The Authors

PY - 2022/7/27

Y1 - 2022/7/27

N2 - During courtship, male butterflies of many species produce androconial secretions containing male sex pheromones (MSPs) that communicate species identity and affect female choice. MSPs are thus likely candidates as reproductive barriers, yet their role in speciation remains poorly studied. Although Heliconius butterflies are a model system in speciation, their MSPs have not been investigated from a macroevolutionary perspective. We use GC/MS to characterize male androconial secretions in 33 of the 69 species in the Heliconiini tribe. We found these blends to be species-specific, consistent with a role in reproductive isolation. We detected a burst in blend diversification rate at the most speciose genus, Heliconius; a consequence of Heliconius and Eueides species using a fatty acid (FA) metabolic pathway to unlock more complex blends than basal Heliconiini species, whose secretions are dominated by plant-like metabolites. A comparison of 10 sister species pairs demonstrates a striking positive correlation between blend dissimilarity and range overlap, consistent with character displacement or reinforcement in sympatry. These results demonstrate for the first time that MSP diversification can promote reproductive isolation across this group of butterflies, showcasing how implementation of an ancestral trait, the co-option of the FA metabolic pathway for pheromone production, can facilitate rapid speciation.

AB - During courtship, male butterflies of many species produce androconial secretions containing male sex pheromones (MSPs) that communicate species identity and affect female choice. MSPs are thus likely candidates as reproductive barriers, yet their role in speciation remains poorly studied. Although Heliconius butterflies are a model system in speciation, their MSPs have not been investigated from a macroevolutionary perspective. We use GC/MS to characterize male androconial secretions in 33 of the 69 species in the Heliconiini tribe. We found these blends to be species-specific, consistent with a role in reproductive isolation. We detected a burst in blend diversification rate at the most speciose genus, Heliconius; a consequence of Heliconius and Eueides species using a fatty acid (FA) metabolic pathway to unlock more complex blends than basal Heliconiini species, whose secretions are dominated by plant-like metabolites. A comparison of 10 sister species pairs demonstrates a striking positive correlation between blend dissimilarity and range overlap, consistent with character displacement or reinforcement in sympatry. These results demonstrate for the first time that MSP diversification can promote reproductive isolation across this group of butterflies, showcasing how implementation of an ancestral trait, the co-option of the FA metabolic pathway for pheromone production, can facilitate rapid speciation.

KW - chemical ecology

KW - macroevolution

KW - reproductive isolation

KW - sympatric speciation

UR - http://www.scopus.com/inward/record.url?scp=85135112395&partnerID=8YFLogxK

U2 - 10.1098/rspb.2022.0474

DO - 10.1098/rspb.2022.0474

M3 - Article

C2 - 35892212

AN - SCOPUS:85135112395

SN - 0962-8452

VL - 289

JO - Proceedings of the Royal Society B

JF - Proceedings of the Royal Society B

IS - 1979

M1 - 20220474

ER -