skip to main content

Attention:

The NSF Public Access Repository (PAR) system and access will be unavailable from 8:00 PM ET on Friday, March 21 until 8:00 AM ET on Saturday, March 22 due to maintenance. We apologize for the inconvenience.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


Title: bric à brac controls sex pheromone choice by male European corn borer moths
Abstract

The sex pheromone system of ~160,000 moth species acts as a powerful form of assortative mating whereby females attract conspecific males with a species-specific blend of volatile compounds. Understanding how female pheromone production and male preference coevolve to produce this diversity requires knowledge of the genes underlying change in both traits. In the European corn borer moth, pheromone blend variation is controlled by two alleles of an autosomal fatty-acyl reductase gene expressed in the female pheromone gland (pgFAR). Here we show that asymmetric male preference is controlled bycis-acting variation in a sex-linked transcription factor expressed in the developing male antenna,bric à brac(bab). A genome-wide association study of preference using pheromone-trapped males implicates variation in the 293 kbbabintron 1, rather than the coding sequence. Linkage disequilibrium betweenbabintron 1 andpgFARfurther validatesbabas the preference locus, and demonstrates that the two genes interact to contribute to assortative mating. Thus, lack of physical linkage is not a constraint for coevolutionary divergence of female pheromone production and male behavioral response genes, in contrast to what is often predicted by evolutionary theory.

  more » « less
PAR ID:
10228264
Author(s) / Creator(s):
; ; ; ; ; ; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Nature Communications
Volume:
12
Issue:
1
ISSN:
2041-1723
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; ; ( , Pest Management Science)
    Abstract BACKGROUND

    Geographic variation in male response to sex pheromone lures has been studied in the field in a number of moth species. However, only a few studies have investigated geographic variation in female calling and sex pheromone under field conditions. For an effective field implementation of sex pheromone lures, it is essential to know the local sex pheromone blend and local timing of sexual communication. We investigated the level and extent of geographic variation in the sexual communication of the important agricultural pestHelicoverpa armigera(Lepidoptera, Noctuidae) in three continents.

     RESULTS

    We found there is no genetic variation in the calling behavior ofH. armigera. In the female sex pheromone, we found more between‐population variation than within‐population variation. In male response experiments, we found geographic variation as well. Strikingly, when adding the antagonistic compound Z11‐16:OAc to the pheromone blend ofH. armigera, significantly fewer males were caught in Australia and China, but not in Spain. This variation is likely not only due to local environmental conditions, such as photoperiod and temperature, but also to the presence of other closely related species with which communication interference may occur.

     Conclusion

    Finding geographic variation in both the female sexual signal and the male response in this pest calls for region‐specific pheromone lures. Our study shows that the analysis of geographic variation in moth female sex pheromones as well as male responses is important for effectively monitoring pest species that occur around the globe. © 2020 The Authors.Pest Management Sciencepublished by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

     
    more » « less
  2. ; ; ; ; ; ; ; ( , Molecular Ecology)
    Abstract

    Patterns of mating for the European corn borer (Ostrinia nubilalis) moth depend in part on variation in sex‐pheromone blend. The ratio of (E)‐11‐ and (Z)‐11‐tetradecenyl acetate (E11‐ and Z11‐14:OAc) in the pheromone blend that females produce and males respond to differs between strains ofO. nubilalis. Populations also vary in female oviposition preference for and larval performance on maize (C4) and nonmaize (C3) host plants. The relative contributions of sexual and ecological trait variation to the genetic structure ofO. nubilalisremains unknown. Host‐plant use (13C/14C ratios) and genetic differentiation were estimated among sympatric E and Z pheromone strainO. nubilalismales collected in sex‐pheromone baited traps at 12 locations in Pennsylvania and New York between 2007 and 2010. Among genotypes at 65 single nucleotide polymorphism marker loci, variance at a position in the pheromone gland fatty acyl‐reductase (pgfar) gene at the locus responsible for determining female pheromone ratio (Pher) explained 64% of the total genetic differentiation between males attracted to different pheromones (male response,Resp), providing evidence of sexual inter‐selection at these unlinked loci. Principal coordinate, Bayesian clustering, and distance‐based redundancy analysis (dbRDA) demonstrate that host plant history or geography does not significantly contribute to population variation or differentiation among males. In contrast, these analyses indicate that pheromone response andpgfar‐defined strain contribute significantly to population genetic differentiation. This study suggests that behavioural divergence probably plays a larger role in driving genetic variation compared to host plant‐defined ecological adaptation.

     
    more » « less
  3. ; ; ; ; ; ; ; ; ; ( , Proceedings of the National Academy of Sciences)
    Mating cues evolve rapidly and can contribute to species formation and maintenance. However, little is known about how sexual signals diverge and how this variation integrates with other barrier loci to shape the genomic landscape of reproductive isolation. Here, we elucidate the genetic basis of ultraviolet (UV) iridescence, a courtship signal that differentiates the males of Colias eurytheme butterflies from a sister species, allowing females to avoid costly heterospecific matings. Anthropogenic range expansion of the two incipient species established a large zone of secondary contact across the eastern United States with strong signatures of genomic admixtures spanning all autosomes. In contrast, Z chromosomes are highly differentiated between the two species, supporting a disproportionate role of sex chromosomes in speciation known as the large-X (or large-Z) effect. Within this chromosome-wide reproductive barrier, linkage mapping indicates that cis- regulatory variation of bric a brac ( bab ) underlies the male UV-iridescence polymorphism between the two species. Bab is expressed in all non-UV scales, and butterflies of either species or sex acquire widespread ectopic iridescence following its CRISPR knockout, demonstrating that Bab functions as a suppressor of UV-scale differentiation that potentiates mating cue divergence. These results highlight how a genetic switch can regulate a premating signal and integrate with other reproductive barriers during intermediate phases of speciation. 
    more » « less
  4. ; ; ( , Integrative Organismal Biology)
    null (Ed.)
    Synopsis Sound production in tiger moths (Erebidae: Arctiinae) plays a role in natural selection. Some species use tymbal sounds as jamming signals avoiding bat predation. High duty cycle signals have the greatest efficacy in this regard. Tiger moth sounds can also be used for intraspecific communication. Little is known about the role of sound in the mating behavior of jamming species or the signal preferences underlying mate choice. We recorded sound production during the courtship of two high duty cycle arctiines, Bertholdia trigona and Carales arizonensis. We characterized variation in their acoustic signals, measured female preference for male signals that vary in duty cycle, and performed female choice experiments to determine the effect of male duty cycle on the acceptance of male mates. Although both species produced sound during courtship, the role of acoustic communication appears different between the species. Bertholdia trigona was acoustically active in all intraspecific interactions. Females preferred and ultimately mated with males that produced higher duty cycles. Muted males were never chosen. In C. arizonensis however, sound emissions were limited during courtship and in some successful matings no sound was detected. Muted and clicking males were equally successful in female mate-choice experiments, indicating that acoustic communication is not essential for mating in C. arizonensis. Our results suggest that in B. trigona natural and sexual selection may work in parallel, to favor higher duty cycle clicking. 
    more » « less
  5. ; ; ; ; ( , Journal of Evolutionary Biology)
    Abstract

    Variation in temperature can affect the expression of a variety of important fitness‐related behaviours, including those involved with mate attraction and selection, with consequences for the coordination of mating across variable environments. We examined how temperature influences the expression of male mating signals and female mate preferences—as well as the relationship between how male signals and female mate preferences change across temperatures (signal–preference temperature coupling)—inEnchenopa binotatatreehoppers. These small plant‐feeding insects communicate using plantborne vibrations, and our field surveys indicate they experience significant natural variation in temperature during the mating season. We tested for signal–preference temperature coupling in four populations ofE. binotataby manipulating temperature in a controlled laboratory environment. We measured the frequency of male signals—the trait for which females show strongest preference—and female peak preference—the signal frequency most preferred by females—across a range of biologically relevant temperatures (18°C–36°C). We found a strong effect of temperature on both male signals and female preferences, which generated signal–preference temperature coupling within each population. Even in a population in which male signals mismatched female preferences, the temperature coupling reinforces predicted directional selection across all temperatures. Additionally, we found similar thermal sensitivity in signals and preferences across populations even though populations varied in the mean frequency of male signals and female peak preference. Together, these results suggest that temperature variation should not affect the action of sexual selection via female choice, but rather should reinforce stabilizing selection in populations with signal–preference matches, and directional selection in those with signal–preference mismatches. Finally, we do not predict that thermal variation will disrupt the coordination of mating in this species by generating signal–preference mismatches at thermal extremes.

     
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email