@article{liu_heath_zhang_wijk_wang_buellesbach_wada-katsumata_groot_schal_2023, title={A mosaic of endogenous and plant-derived courtship signals in moths}, volume={33}, ISSN={["1879-0445"]}, url={https://doi.org/10.1016/j.cub.2023.07.010}, DOI={10.1016/j.cub.2023.07.010}, abstractNote={Insects rely on olfaction to guide a wide range of adaptive behaviors, including mate and food localization, mate choice, oviposition site selection, kin recognition, and predator avoidance.1Wyatt T.D. Pheromones and Animal Behaviour: Communication by Smell and Taste. Cambridge University Press, 2003Crossref Google Scholar In nocturnal insects, such as moths2Allison J.D. Cardé R.T. Pheromone Communication in Moths: Evolution, Behavior, and Application. University of California Press, 2016Crossref Google Scholar and cockroaches,3Gemeno C. Schal C. Sex pheromones of cockroaches.in: Cardé R.T. Millar J.G. Advances in Insect Chemical Ecology. Cambridge University Press, 2004: 179-247Crossref Google Scholar mate finding is stimulated predominantly by long-range species-specific sex pheromones, typically emitted by females. During courtship, at close range, males in most moth species emit a blend of pheromone compounds from an everted, often large, pheromone gland. While long-distance communication with sex pheromones has been remarkably well characterized in thousands of moth species,2Allison J.D. Cardé R.T. Pheromone Communication in Moths: Evolution, Behavior, and Application. University of California Press, 2016Crossref Google Scholar,4El-Sayed A.M. The Pherobase: Database of Insect Pheromones and Semiochemicals.2012http://www.pherobase.comGoogle Scholar close-range chemosensory sexual communication remains poorly understood. We reveal that in the moth Chloridea virescens, the male pheromone consists of three distinct classes of compounds: de novo biosynthesized alcohols, aldehydes, acetates, and carboxylic acids that resemble the female's emissions; newly identified compounds that are unique to the male pheromone, such as aliphatic polyunsaturated hydrocarbons; and sequestered plant secondary compounds and hormone derivatives, including methyl salicylate (MeSA). Thus, males employ a mosaic pheromone blend of disparate origins that may serve multiple functions during courtship. We show that two olfactory receptors in female antennae are tuned to MeSA, which facilitates female acceptance of the male. Because MeSA is emitted by plants attacked by pathogens and herbivores,5Takabayashi J. Shiojiri K. Multifunctionality of herbivory-induced plant volatiles in chemical communication in tritrophic interactions.Curr. Opin. Insect Sci. 2019; 32: 110-117https://doi.org/10.1016/j.cois.2019.01.003Crossref PubMed Scopus (54) Google Scholar the chemosensory system of female moths was likely already tuned to this plant volatile, and males appear to exploit the female's preadapted sensory bias. Interestingly, while female moths (largely nocturnal) and butterflies (diurnal) diverged in their use of sensory modalities in sexual communication,6Ehlers S. Schulz S. The scent chemistry of butterflies.Nat. Prod. Rep. 2023; 40: 794-818https://doi.org/10.1039/D2NP00067ACrossref PubMed Google Scholar MeSA is used by males of both lineages.}, number={16}, journal={CURRENT BIOLOGY}, author={Liu, Yang and Heath, Jeremy J. and Zhang, Sai and Wijk, Michiel and Wang, Guirong and Buellesbach, Jan and Wada-Katsumata, Ayako and Groot, Astrid T. and Schal, Coby}, year={2023}, month={Aug} }
 @article{zweerus_wijk_schal_groot_2023, title={Diet-derived male sex pheromone compounds affect female choice in a noctuid moth}, volume={13}, ISSN={["2045-2322"]}, DOI={10.1038/s41598-023-47041-8}, abstractNote={AbstractSexual signals often function in species recognition and may also guide mate choice within a species. In noctuid moths, both males and females may exercise mate choice. Females of the tobacco budworm Chloridea virescens prefer to mate with larger males, but the signal(s) underlying female choice remain unknown. Male hairpencil volatiles are emitted during close range courtship displays. However, previously identified male hairpencil volatiles, namely acetate esters, aldehydes, alcohols, and fatty acids, are not associated with female choice. Recently, two new hairpencil compounds were identified that elicit strong electrophysiological responses in female antennae: methyl salicylate (MeSA) and δ-decalactone. In this study, we investigated the effect of larval diet and adult feeding on MeSA and δ-decalactone content in hairpencils and determined whether these compounds are involved in female choice. We found that larval diet affected MeSA content in hairpencils, but not δ-decalactone. Conversely, adult feeding affected the level of δ-decalactone, but not MeSA: sugar-water feeding increased δ-decalactone content compared to plain water. In two-choice assays, females mated more with males that had higher amounts of δ-decalactone, and less with males with higher amounts of MeSA.}, number={1}, journal={SCIENTIFIC REPORTS}, author={Zweerus, Naomi L. and Wijk, Michiel and Schal, Coby and Groot, Astrid T.}, year={2023}, month={Nov} }
 @article{fouchier_fruitet_lievers_kuperus_emerson_gould_heckel_groot_2023, title={Lipases and carboxylesterases affect moth sex pheromone compounds involved in interspecific mate recognition}, volume={14}, ISSN={["2041-1723"]}, DOI={10.1038/s41467-023-43100-w}, abstractNote={AbstractMoth sex pheromones are a classical model for studying sexual selection. Females typically produce a species-specific pheromone blend that attracts males. Revealing the enzymes involved in the interspecific variation in blend composition is key for understanding the evolution of these sexual communication systems. The nature of the enzymes involved in the variation of acetate esters, which are prominent compounds in moth pheromone blends, remains unclear. We identify enzymes involved in acetate degradation using two closely related moth species: Heliothis (Chloridea) subflexa and H. (C.) virescens, which have different quantities of acetate esters in their sex pheromone. Through comparative transcriptomic analyses and CRISPR/Cas9 knockouts, we show that two lipases and two esterases from H. virescens reduce the levels of pheromone acetate esters when expressed in H. subflexa females. Together, our results show that lipases and carboxylesterases are involved in tuning Lepidoptera pheromones composition.}, number={1}, journal={NATURE COMMUNICATIONS}, author={Fouchier, Arthur and Fruitet, Elise and Lievers, Rik and Kuperus, Peter and Emerson, Jennifer and Gould, Fred and Heckel, David G. and Groot, Astrid T.}, year={2023}, month={Nov} }
 @article{zweerus_wijk_schal_groot_2021, title={Experimental evidence for female mate choice in a noctuid moth}, volume={179}, ISSN={["1095-8282"]}, DOI={10.1016/j.anbehav.2021.06.022}, abstractNote={Sexual signal evolution is shaped by whether only one or both sexes execute mate choice. When mate choice by both sexes is considered, the same signalling modality is generally inferred for males and females. In the noctuid moth Chloridea (Heliothis) virescens (Lepidoptera: Noctuidae), both sexes may be signallers and responders, as both emit a sex-specific pheromone. Male mate choice is based on the female sex pheromone, perceived via the antennae, and has been well documented. However, whether females choose partners and whether their choice is based on the male pheromone are unknown. Since female mate choice is expected when males vary in quality, we reared males on two different larval diets that affected their size, which correlated positively with their fitness. When given a choice, more females mated with larger than with smaller males, and these females produced more eggs and larvae. Female choice was not affected by the absolute amount or composition of the male pheromone. Moreover, we found that antennaless females mated as readily as intact females, indicating that antennal sensory input is not required for females to mate. To determine whether females make an active choice, we studied courtship behaviour in detail and observed that females determined the outcome of courtship by moving away from the male (avoidance) or by facilitating copulation with an abdominal bend (acceptance). Additionally, we discovered that tactile sensory stimuli may be involved during courtship. Because tactile interactions may mediate contact-based (chemical) communication, we also investigated putative pheromone components on moth legs, but found no differences between the sexes. Together, our study is the first comprehensive investigation of female mate choice in a heliothine moth.}, journal={ANIMAL BEHAVIOUR}, author={Zweerus, Naomi L. and Wijk, Michiel and Schal, Coby and Groot, Astrid T.}, year={2021}, month={Sep}, pages={1–13} }
 @article{nojima_classen_groot_schal_2018, title={Qualitative and quantitative analysis of chemicals emitted from the pheromone gland of individual Heliothis subflexa females}, volume={13}, ISSN={1932-6203}, url={http://dx.doi.org/10.1371/journal.pone.0202035}, DOI={10.1371/journal.pone.0202035}, abstractNote={The chemicals emitted from the sex pheromone gland of individual Heliothis subflexa females were sampled using a short section of thick-film megabore fused silica capillary column, and the pheromone glands of the same females were extracted after the effluvia collection. Both samples were treated with a silylation reagent, and then subjected to gas chromatography-chemical ionization-mass spectrometry for quantitative and qualitative analysis of all components. The total amount of all 11 components emitted from the glands of calling females was 153 ng/female/hr, which was substantially higher than previously reported. The ratios of the pheromone components in the volatile emissions and pheromone gland extracts were generally similar to previous studies, but with notable differences. The collections of volatiles and gland extractions contained, respectively: Z9-14:Ald (1.57%, 1.35%), 14:Ald (3.78%, 1.51%), Z7 + Z9-16:Ald (9.60%, 3.59%), Z11-16:Ald (76.14%, 18.94%), 16:Ald (2.95%, 2.17%), Z9-16:OH (0.07%, 7.21%), Z11-16:OH (1.11%, 49.04%), Z7-16:OAc (0.48%, 1.73%), Z9-16:OAc (1.32%, 4.02%), and Z11-16:OAc (2.98%, 10.43%). The thick-film megabore column is an efficient approach for sampling the headspace for semiochemicals.}, number={8}, journal={PLOS ONE}, publisher={Public Library of Science (PLoS)}, author={Nojima, Satoshi and Classen, Alice and Groot, Astrid T. and Schal, Coby}, editor={Hull, J JoeEditor}, year={2018}, month={Aug}, pages={e0202035} }
 @article{hosseini_goldansaz_menken_wijk_roessingh_groot_2017, title={Field Attraction of Carob Moth to Host Plants and Conspecific Females}, volume={110}, ISSN={["1938-291X"]}, DOI={10.1093/jee/tox218}, abstractNote={Abstract The carob moth, Ectomyelois ceratoniae (Zeller; Lepidoptera: Pyralidae), is a devastating pest in high-value crops around the world. An efficient sex pheromone attractant is still missing for the management of this pest, because the major pheromone component is unstable. Host plant volatiles attract herbivore insects and have shown to have good potential to be exploited as alternatives or supplements to sex pheromones.To explore this possibility in carob moth, we assessed the attraction of moths to the volatiles of mature pistachio and different fruit stages of pomegranate, alone and in combination with virgin females, using sticky delta traps in pomegranate orchards of Iran. Traps baited with mature pomegranates, whether uncracked or cracked, infested or uninfested, caught significantly larger numbers of male and both mated and virgin female carob moths than unbaited traps. Traps baited with headspace extract of cracked pomegranate only caught mated females, while mature pistachio only attracted males. Pomegranate flowers, unripe pomegranate, and headspace extract of pistachio did not attract moths. Traps baited with cracked fruit caught more mated females than traps baited with uncracked fruit. Males were attracted similarly to traps baited with cracked-infested pomegranate as to traps baited with virgin females alone. Interestingly, the combination of cracked pomegranate and virgin female enhanced the attraction of virgin females.Together, our results show that volatiles from cracked pomegranates alone or in combination with female sex pheromone have great potential for application in pest management programs of carob moth.}, number={5}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, author={Hosseini, Seyed Ali and Goldansaz, Seyed Hossein and Menken, Steph B. J. and Wijk, Michiel and Roessingh, Peter and Groot, Astrid T.}, year={2017}, month={Oct}, pages={2076–2083} }
 @article{van wijk_heath_lievers_schal_groot_2017, title={Proximity of signallers can maintain sexual signal variation under stabilizing selection}, volume={7}, ISSN={2045-2322}, url={http://dx.doi.org/10.1038/s41598-017-17327-9}, DOI={10.1038/s41598-017-17327-9}, abstractNote={AbstractHow sexual communication systems can evolve under stabilizing selection is still a paradox in evolutionary biology. In moths, females emit a species-specific sex pheromone, consisting of a blend of biochemically related components, to which males are attracted. Although males appear to exert strong stabilizing selection on female pheromone, these blends seem to have evolved rapidly, as evidenced by ~120,000 moth species. Here we propose and test a “proximity model” wherein two females that vary in their relative attractiveness to males, can both benefit from calling in close proximity to each other. In a field study, we show that (1) artificially selected unattractive females can achieve mating rates comparable to attractive females if they signal in close proximity to attractive females, and (2) attractive females benefit from higher mating rates when signalling in close proximity to unattractive females. We propose that frequency-dependent behavioural and spatial interactions can sustain signal variation within populations even when these signals are under stabilizing selection.}, number={1}, journal={Scientific Reports}, publisher={Springer Science and Business Media LLC}, author={van Wijk, Michiel and Heath, Jeremy and Lievers, Rik and Schal, Coby and Groot, Astrid T.}, year={2017}, month={Dec} }
 @article{hosseini_van wijk_ke_goldansaz_schal_groot_2016, title={Experimental evidence for chemical mate guarding in a moth}, volume={6}, ISSN={2045-2322}, url={http://dx.doi.org/10.1038/srep38567}, DOI={10.1038/srep38567}, abstractNote={AbstractIn polyandrous species, males seek to maximize their reproductive output by monopolizing their mate. Often the male transfers substances to the female that suppress her sexual receptivity or antagonize the behavior of competing males; both are usually transferred in seminal fluids and represent forms of chemical mate guarding. In moths, more long-range female sex pheromones have been identified than in any other animal group, and males often display with close-range sex pheromones, yet odor-based post-copulatory mate guarding has not been described in moths so far. We tested the hypothesis that the male sex pheromone in the noctuid moth Heliothis virescens perfumes the female and functions as an anti-aphrodisiac. Indeed, virgin females perfumed with male pheromone extract, or with its main component, mated significantly less than control virgin females, and this effect persisted for two successive nights. This chemical mate guarding strategy was disadvantageous for H. virescens females, because the reproductive output of twice-mated females was significantly higher than that of once-mated females. Since the female and male sex pheromones are biosynthetically related in this and other moth species, chemical mate guarding may also impose selection pressure on the long-range female sex pheromone channel and consequently affect the evolution of sexual communication.}, number={1}, journal={Scientific Reports}, publisher={Springer Science and Business Media LLC}, author={Hosseini, Seyed Ali and van Wijk, Michiel and Ke, Gao and Goldansaz, Seyed Hossein and Schal, Coby and Groot, Astrid T.}, year={2016}, month={Dec} }
 @article{groot_schöfl_inglis_donnerhacke_classen_schmalz_santangelo_emerson_gould_schal_et al._2014, title={Within-population variability in a moth sex pheromone blend: genetic basis and behavioural consequences}, volume={281}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2013.3054}, DOI={10.1098/rspb.2013.3054}, abstractNote={Evolutionary diversification of sexual communication systems in moths is perplexing because signal and response are under stabilizing selection in many species, and this is expected to constrain evolutionary change. In the mothHeliothis virescens, we consistently found high phenotypic variability in the female sex pheromone blend within each of four geographically distant populations. Here, we assess the heritability, genetic basis and behavioural consequences of this variation. Artificial selection with field-collected moths dramatically increased the relative amount of the saturated compound 16:Ald and decreased its unsaturated counterpart Z11–16:Ald, the major sex pheromone component (high line). In a cross between the high- and low-selected lines, one quantitative trait locus (QTL) explained 11–21% of the phenotypic variance in the 16:Ald/Z11–16:Ald ratio. Because changes in activity of desaturase enzymes could affect this ratio, we measured their expression levels in pheromone glands and mapped desaturase genes onto our linkage map. A delta-11-desaturase had lower expression in females producing less Z11–16:Ald; however, this gene mapped to a different chromosome than the QTL. A model in which the QTL is a trans-acting repressor of delta-11 desaturase expression explains many features of the data. Selection favouring heterozygotes which produce more unsaturated components could maintain a polymorphism at this locus.}, number={1779}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Groot, Astrid T. and Schöfl, Gerhard and Inglis, Ollie and Donnerhacke, Susanne and Classen, Alice and Schmalz, Antje and Santangelo, Richard G. and Emerson, Jennifer and Gould, Fred and Schal, Coby and et al.}, year={2014}, month={Mar}, pages={20133054} }
 @article{gould_estock_hillier_powell_groot_ward_emerson_schal_vickers_2010, title={Sexual isolation of male moths explained by a single pheromone response QTL containing four receptor genes}, volume={107}, ISSN={["0027-8424"]}, DOI={10.1073/pnas.0910945107}, abstractNote={
            Long distance sexual communication in moths has fascinated biologists because of the complex, precise female pheromone signals and the extreme sensitivity of males to specific pheromone molecules. Progress has been made in identifying some genes involved in female pheromone production and in male response. However, we have lacked information on the genetic changes involved in evolutionary diversification of these mate-finding mechanisms that is critical to understanding speciation in moths and other taxa. We used a combined quantitative trait locus (QTL) and candidate gene approach to determine the genetic architecture of sexual isolation in males of two congeneric moths,
            Heliothis subflexa
            and
            Heliothis virescens
            . We report behavioral and neurophysiological evidence that differential male responses to three female-produced chemicals (
            Z
            9-14:Ald,
            Z
            9-16:Ald,
            Z
            11-16:OAc) that maintain sexual isolation of these species are all controlled by a single QTL containing at least four odorant receptor genes. It is not surprising that pheromone receptor differences could control
            H. subflexa
            and
            H. virescens
            responses to
            Z
            9-16:Ald and
            Z
            9-14:Ald, respectively. However, central rather than peripheral level control over the positive and negative responses of
            H. subflexa
            and
            H. virescens
            to
            Z
            11-16:OAc had been expected. Tight linkage of these receptor genes indicates that mutations altering male response to complex blends could be maintained in linkage disequilibrium and could affect the speciation process. Other candidate genes such as those coding for pheromone binding proteins did not map to this QTL, but there was some genetic evidence of a QTL for response to
            Z
            11-16:OH associated with a sensory neuron membrane protein gene.
          }, number={19}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Gould, Fred and Estock, Marie and Hillier, N. Kirk and Powell, Bekah and Groot, Astrid T. and Ward, Catherine M. and Emerson, Jennifer L. and Schal, Coby and Vickers, Neil J.}, year={2010}, month={May}, pages={8660–8665} }
 @article{blanco_andow_abel_sumerford_hernandez_lópez_adams_groot_leonard_parker_et al._2009, title={<I>Bacillus thuringiensis</I> Cry1Ac Resistance Frequency in Tobacco Budworm (Lepidoptera: Noctuidae)}, volume={102}, ISSN={0022-0493 0022-0493}, url={http://dx.doi.org/10.1603/029.102.0149}, DOI={10.1603/029.102.0149}, abstractNote={ABSTRACT 
 The tobacco budworm, Heliothis virescens (F.) (Lepidoptera Noctuidae), is one of the most important pests of cotton, Gossypium hirsutum L., that has become resistant to a wide range of synthetic insecticides. Cry1Ac-expressing cotton has proven its effectiveness against this insect since its introduction in North America in 1996. However, the constant exposure of tobacco budworm to this protein toxin may result in the development of resistance to it. To estimate the frequency of alleles that confer resistance to a 1.0 µg of Bacillus thuringiensis Cry1Ac diagnostic concentration in field-collected insects, the second generation (F2) of 1,001 single-pair families from seven geographical regions representing 2,202 alleles from natural populations was screened in 2006 and 2007 without finding major resistant alleles. Neonates of 56 single-pair families were able to develop to second instar on the diagnostic concentration in the initial screen, but only seven of these lines did so again in a second confirmatory screen. Minor resistance alleles to Cry1Ac may be quite common in natural populations of H. virescens. Our estimated resistance allele frequencies (0.0036 – 0.0263) were not significantly different from a previously published estimate from 1993. There is no evidence that H. virescens populations have become more resistant to Cry1Ac.}, number={1}, journal={Journal of Economic Entomology}, publisher={Oxford University Press (OUP)}, author={Blanco, Carlos A. and Andow, David A. and Abel, Craig A. and Sumerford, Douglas V. and Hernandez, Gerardo and López, Juan D., Jr and Adams, Larry and Groot, Astrid and Leonard, Rogers and Parker, Roy and et al.}, year={2009}, month={Feb}, pages={381–387} }
 @misc{groot_inglis_bowdridge_santangelo_blanco_lopez_teran vargas_gould_schal_2009, title={GEOGRAPHIC AND TEMPORAL VARIATION IN MOTH CHEMICAL COMMUNICATION}, volume={63}, ISSN={["1558-5646"]}, DOI={10.1111/j.1558-5646.2009.00702.x}, abstractNote={In moth pheromone communication signals, both quantitative and qualitative intraspecific differences have been found across geographic regions. Such variation has generally been hypothesized to be due to selection, but evidence of genetic control of these differences is largely lacking. To explore the patterns of variation in pheromone signals, we quantified variation in the female sex pheromone blend and male responses of two closely related noctuid moth species in five different geographic regions for 2–3 consecutive years. We found significant variation in the ratios of sex pheromone blend components as well as in male response, not only between geographic regions but also within a region between consecutive years. The temporal variation was of a similar magnitude as the geographic variation. As far as we know, this is the first study reporting such temporal variation in moth chemical communication systems. The geographic variation seems to at least partly be controlled by genetic factors, and to be correlated with the quality of the local chemical environment. However, the pattern of temporal variation within populations suggests that optimization of the pheromonal signal also may be driven by within-generation physiological adjustments by the moths in response to their experience of the local chemical environment.}, number={8}, journal={EVOLUTION}, author={Groot, Astrid T. and Inglis, Olive and Bowdridge, Scott and Santangelo, Richard G. and Blanco, Carlos and Lopez, Juan D., Jr. and Teran Vargas, Antonio and Gould, Fred and Schal, Coby}, year={2009}, month={Aug}, pages={1987–2003} }
 @article{groot_estock_horovitz_hamilton_santangelo_schal_gould_2009, title={QTL analysis of sex pheromone blend differences between two closely related moths: Insights into divergence in biosynthetic pathways}, volume={39}, ISSN={["1879-0240"]}, DOI={10.1016/j.ibmb.2009.05.002}, abstractNote={To understand the evolution of premating signals in moths, it is important to know the genetic basis of these signals. We conducted Quantitative Trait Locus (QTL) analysis by hybridizing two noctuid moth species, Heliothis virescens (Hv) and Heliothis subflexa (Hs), and backcrossing the F1 females to males of both parental species. One of these backcrosses (F1 × Hs) was a biological replicate of our previous study (Sheck et al., 2006) and served to test the robustness of our previous findings. The backcross to Hv was designed to reveal QTL with recessive inheritance of the Hv character state. This study confirms previously discovered QTL, but also reports new QTL. Most importantly, we found relatively large QTL affecting Z9-16:Ald, the critical sex pheromone component of Hs. For Z9-14:Ald, the critical sex pheromone component of Hv, as well as for the minor pheromone compound 14:Ald, we found QTL in which the change in pheromone ratio was opposite-to-expected. Linking QTL to the biosynthetic pathways of the pheromone compounds of Hv and Hs implicates several candidate genes in the divergence of these premating signals, the most important of which are acetyl transferase, one or more desaturase(s), and a fatty acyl reductase or alcohol oxidase.}, number={8}, journal={INSECT BIOCHEMISTRY AND MOLECULAR BIOLOGY}, author={Groot, Astrid T. and Estock, Marie L. and Horovitz, Joy L. and Hamilton, Jennifer and Santangelo, Richard G. and Schal, Coby and Gould, Fred}, year={2009}, month={Aug}, pages={568–577} }
 @article{blanco_perera_groot_hernandez_teran-vargas_2008, title={Paternity Allocation in a Mutant Heliothis virescens Colony}, volume={33}, ISSN={["2162-2647"]}, DOI={10.3958/0147-1724-33.4.253}, abstractNote={Abstract Tobacco budworm, Heliothis virescens (F.) (Lepidoptera: Noctuidae), females can copulate multiple times creating the possibility for sperm competition. We used a colony lacking wild pigmentation on the wings (albino-type) for an experiment in which females double mated. Females copulated 2 days apart with two, 2-day-old males, one albino-type and one wild-type, or in the opposite sequence. A third of the females produced offspring from the first mate, and this group was significantly biased toward producing albino-type compared to wild-type progeny. A fourth of the females produced offspring from the second male exclusively and within this group was a significant bias toward wild-type compared to albino-type progeny. Almost half of the females produced offspring sired in equal proportions by both males simultaneously or in alternated paternities throughout all the reproductive life. These results suggest that regardless of the order in which moths mated, wild-type sperm had potential superior competitiveness. Therefore, sperm precedence is not the main driving force behind the paternity allocation mechanism in this strain of tobacco budworm.}, number={4}, journal={SOUTHWESTERN ENTOMOLOGIST}, author={Blanco, Carlos A. and Perera, Omaththage P. and Groot, Astrid and Hernandez, Gerardo and Teran-Vargas, Antonio P.}, year={2008}, month={Dec}, pages={253–263} }
 @article{groot_santangelo_ricci_brownie_gould_schal_2007, title={Differential attraction of Heliothis subflexa males to synthetic pheromone lures in eastern US and western Mexico}, volume={33}, ISSN={["1573-1561"]}, DOI={10.1007/s10886-006-9233-6}, abstractNote={The mate attraction signal of Heliothis subflexa (Hs) females consists of a multicomponent sex pheromone blend. In this study, we assessed the intraspecific importance of three groups of compounds found in Hs pheromone glands: three acetate esters (Z7-16:OAc, Z9-16:OAc, and Z11-16:OAc), two 14-carbon aldehydes (14:Ald and Z9-14:Ald), and one 16-carbon alcohol (Z11-16:OH). Because the relative importance of pheromone components may vary in different regions, we conducted experiments in Eastern US (North Carolina) and Western Mexico (Jalisco). Our experiments in Eastern US showed that when the acetates were omitted from a 7-component blend in rubber septa, fewer males were caught in cone traps. Subsequent experiments conducted both in Eastern US and Western Mexico indicated that the addition of Z9-16:OAc alone does not increase attraction of male Hs, while Z11-16:OAc does. The Hs male response to Z7-16:OAc differed between the two regions. In Eastern US, significantly more males were attracted to a minimal three-component blend to which Z7-16:OAc was added, but this was not the case in Western Mexico. The two 14-carbon aldehydes also showed differential attraction between the two regions. 14:Ald and Z9-14:Ald appeared not to play any role in the sexual communication of Hs in Eastern US, but reduced trap catches in Western Mexico. The alcohol Z11-16:OH was tested in two concurrent dose-response studies with Hs males in Western Mexico, one using a minimal blend and one using a complete blend. The minimal three-component blend provided a more discriminating tool for delineating dose-response effects of Z11-16:OH than the seven-component blend. In the minimal blend, the optimal dose of Z11-16:OH was 1%, while in the complete blend similar numbers of males were caught when the alcohol ranged from 1 to 25%.}, number={2}, journal={JOURNAL OF CHEMICAL ECOLOGY}, author={Groot, A. T. and Santangelo, R. G. and Ricci, E. and Brownie, C. and Gould, F. and Schal, Coby}, year={2007}, month={Feb}, pages={353–368} }
 @article{groot_horovitz_hamilton_santangelo_schal_gould_2006, title={Experimental evidence for interspecific directional selection on moth pheromone communication}, volume={103}, ISSN={["0027-8424"]}, DOI={10.1073/pnas.0508609103}, abstractNote={The chemical composition of the sexual communication signals of female moths is thought to be under strong stabilizing selection, because females that produce atypical pheromone blends suffer lower success in finding mates. This intraspecific selection pressure cannot explain the high diversity of moth pheromone blends found in nature. We conducted experiments to determine whether communication interference from males of closely related species could exert strong enough directional selection to cause evolution of these signals. Attraction and mating success ofHeliothis subflexa(Hs) females with a normal quantitative trait locus for production of acetate pheromone components (norm-OAc) were compared with Hs females with an introgressed quantitative trait locus fromHeliothis virescens(Hv) that dramatically decreased the amount of acetate esters in their pheromone glands (low-OAc). In field experiments with natural Hv and Hs populations, 10 times more Hv males were captured in traps baited with live low-OAc Hs females than in traps with norm-OAc Hs females. This pattern was confirmed in mate-choice assays in cages. Hybrids resulting from Hv–Hs matings have effectively zero fitness in the field. Combining our results with the extensive data set gathered in the past 40 years on the reproductive biology of Hv, we can quantitatively estimate that the directional selection exerted by Hv males on Hs females to produce relatively high amounts (>5%) of acetates can range from 0.135 to 0.231. Such intense interspecific selection may counteract intraspecific stabilizing selection that impedes evolutionary changes in pheromone blends and could lead to diversification of sexual signals.}, number={15}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Groot, AT and Horovitz, JL and Hamilton, J and Santangelo, RG and Schal, C and Gould, F}, year={2006}, month={Apr}, pages={5858–5863} }
 @article{groot_fan_brownie_jurenka_gould_schal_2005, title={Effect of PBAN on pheromone production by mated Heliothis virescens and Heliothis subflexa females}, volume={31}, ISSN={["1573-1561"]}, DOI={10.1007/s10886-005-0970-8}, abstractNote={Mated female Heliothis virescens and H. subflexa were induced to produce sex pheromone during the photophase by injection of pheromone biosynthesis activating neuropeptide (PBAN). When injected with 1 pmol Hez-PBAN, the total amount of pheromone that could be extracted from glands of mated females during the photophase was similar to that extracted from virgin females in the scotophase. The PBAN-induced profile of pheromone components was compared between mated, PBAN-injected females and virgin females during spring and fall. Virgin females exhibited some differences in the relative composition of the pheromone blend between spring and fall, but no such temporal differences were detected in PBAN-injected, mated females. Because the temporal variation in pheromone blend composition was greater for virgin females than for PBAN-injected females, PBAN can be used to determine a female's native pheromone phenotype. This procedure has the advantages that pheromone glands can be extracted during the photophase, from mated females that have already oviposited.}, number={1}, journal={JOURNAL OF CHEMICAL ECOLOGY}, author={Groot, AT and Fan, YL and Brownie, C and Jurenka, RA and Gould, F and Schal, C}, year={2005}, month={Jan}, pages={14–28} }
 @article{sheck_groot_ward_gemeno_wang_brownie_schal_gould_2006, title={Genetics of sex pheromone blend differences between Heliothis virescens and Heliothis subflexa: a chromosome mapping approach}, volume={19}, ISSN={["1420-9101"]}, DOI={10.1111/j.1420-9101.2005.00999.x}, abstractNote={Abstract
               Males of the noctuid moths, Heliothis virescens and H. subflexa locate mates based on species-specific responses to female-emitted pheromones that are composed of distinct blends of volatile compounds. We conducted genetic crosses between these two species and used AFLP marker-based mapping of backcross families (H. subflexa direction) to determine which of the 30 autosomes in these moths contained quantitative trait loci (QTL) controlling the proportion of specific chemical components in the pheromone blends. Presence/absence of single H. virescens chromosomes accounted for 7–34% of the phenotypic variation among backcross females in seven pheromone components. For a set of three similar 16-carbon acetates, two H. virescens chromosomes interacted in determining their relative amounts within the pheromone gland and together accounted for 53% of the phenotypic variance. Our results are discussed relative to theories about population genetic processes and biochemical mechanisms involved in the evolution of new sexual communication systems.}, number={2}, journal={JOURNAL OF EVOLUTIONARY BIOLOGY}, author={Sheck, AL and Groot, AT and Ward, CM and Gemeno, C and Wang, J and Brownie, C and Schal, C and Gould, F}, year={2006}, month={Mar}, pages={600–617} }
 @article{groot_gemeno_brownie_gould_schal_2005, title={Male and female antennal responses in Heliothis virescens and H subflexa to conspecific and heterospecific sex pheromone compounds}, volume={34}, ISSN={["1938-2936"]}, DOI={10.1603/0046-225X-34.2.256}, abstractNote={Abstract To determine whether Heliothis virescens and H. subflexa, two closely related sympatrically occurring species, differ in their antennal responses to conspecific and heterospecific pheromone compounds, we recorded electroantennogram (EAG) responses of male and female antennae of both species to eight different compounds loaded on filter paper dispensers. If antennal responses were found to differ in the two species, EAG-recordings from F1 hybrids and backcrosses between these species could be used in developing an understanding of the genetic architecture of variation in olfactory signal perception. However, all compounds elicited EAG responses in all male antennae tested, and no quantitative differences in response were found between the two species, except for the response to 1 mg (Z)-11-hexadecenol (Z11–16:OH), which elicited larger EAG responses in H. subflexa than in H. virescens males. This difference is consistent with the idea that this pheromone component is less important in the biology of H. virescens. Female antennae of both species were less responsive to the major sex pheromone compound, (Z)-11-hexadecenal (Z11–16:Ald), than male antennae; 10 μg Z11–16:Ald, which elicited strong EAG responses in males, produced female EAGs similar to control puffs of air. However, higher doses of Z11–16:Ald elicited significant EAG responses in female antennae of both species. Female antennae of both species also responded to most other pheromone compounds, except Z11–16:OH. These results support the hypothesis that autodetection of sex pheromones occurs in females of both H. virescens and H. subflexa. Whether females behaviorally respond to any, or to combinations, of these compounds remains to be elucidated.}, number={2}, journal={ENVIRONMENTAL ENTOMOLOGY}, author={Groot, A and Gemeno, C and Brownie, C and Gould, F and Schal, C}, year={2005}, month={Apr}, pages={256–263} }
 @article{choi_groot_jurenka_2005, title={Pheromone biosynthetic pathways in the moths Heliothis subflexa and Heliothis virescens}, volume={59}, ISSN={["1520-6327"]}, DOI={10.1002/arch.20051}, abstractNote={Sex pheromones of many moth species have relatively simple structures consisting of a hydrocarbon chain with a functional group and one to several double bonds. These sex pheromones are derived from fatty acids through specific biosynthetic pathways. We investigated the incorporation of deuterium-labeled tetradecanoic, hexadecanoic, and octadecanoic acid precursors into pheromone components of Heliothis subflexa and Heliothis virescens. The two species utilize (Z)11-hexadecenal as the major pheromone component, which is produced by Delta11 desaturation of hexadecanoic acid. H. subflexa also produced (Z)11-hexadecanol and (Z)-11-hexadecenyl acetate via Delta11 desaturation. In H. subflexa, octadecanoic acid was used to biosynthesize the minor pheromone components (Z)9-hexadecenal, (Z)9-hexadecenol, and (Z)9-hexadecenyl acetate. These minor components are produced by Delta11 desaturation of octadecanoic acid followed by one round of chain-shortening. In contrast, H. virescens used hexadecanoic acid as a substrate to form (Z)11-hexadecenal and (Z)11-hexadecenol and hexadecenal. H. virescens also produced (Z)9-tetradecenal by Delta11 desaturation of the hexadecanoic acid followed by one round of chain-shortening and reduction. Tetradecanoic acid was not utilized as a precursor to form Z9-14:Ald in H. virescens. This labeling pattern indicates that the Delta11 desaturase is the only active desaturase present in the pheromone gland cells of both species.}, number={2}, journal={ARCHIVES OF INSECT BIOCHEMISTRY AND PHYSIOLOGY}, author={Choi, MY and Groot, A and Jurenka, RA}, year={2005}, month={Jun}, pages={53–58} }
 @article{groot_ward_wang_pokrzywa_o’brien_bennett_kelly_santangelo_schal_gould_2004, title={Introgressing pheromone QTL between species: Towards an evolutionary understanding of differentiation in sexual communication}, volume={30}, ISSN={["1573-1561"]}, DOI={10.1007/s10886-004-7946-y}, abstractNote={As a first step toward understanding how noctuid moths evolve species-specific pheromone communication systems, we hybridized and backcrossed two closely related moth species, Heliothis virescens (Hv) and H. subflexa (Hs), which differ qualitatively and quantitatively in their multi-component sex pheromone blends. We used amplified fragment length polymorphism (AFLP) marker-based mapping of backcross families to determine which of the 30 autosomes in these moths contained quantitative trait loci (QTL) controlling the percentages of specific chemical components in the pheromone blends. In two previous backcrosses to Hs, we found a strong depressive effect of Hv-chromosome 22 on the percentage of three acetate components in the pheromone gland. These acetates are present in Hs and absent in Hv. Here, we describe how we introgressed Hv-chromosome 22 into the genomic background of Hs. Selection for Hv-chromosome 22 started from backcross 3 (BC3) females. All females that had Hv-chromosome 22 and a low percentage of acetates (< 3% of the total amount of pheromone components present) were backcrossed to Hs males. In BC5 to BC8, we determined whether Hv-chromosome 22 was present by a) running only the primer pairs that would yield the markers for that chromosome, and/or b) determining the relative percentages of acetates in the pheromone glands. Either or both genotype and phenotype were used as a criterion to continue to backcross these females to Hs males. In BC9, we confirmed the isolation of Hv-chromosome 22 in the Hs genomic background, and backcrossed the males to Hs females to eliminate the Hv-sex chromosome as well as mitochondrial DNA. The pheromone composition was determined in BC3, BC5, and BC11 females with and without Hv-chromosome 22. All backcross females with Hv-chromosome 22 contained significantly less acetates than females without this chromosome. In addition, BC3 females with Hv-chromosome 22 contained significantly more Z11-16:OH than BC3 females without Hv-chromosome 22. However, in BC5 and BC11 females, the correlation between Z11-16:OH and Hv-chromosome 22 was lost, suggesting that there are separate QTL for the acetates and for Z11-16:OH, and that the relative amount of the alcohol component is only affected in epistasis with other (minor) QTL. Now that we have succeeded in isolating the chromosome that has a major effect on acetate production, we can test in behavioral experiments whether the presence of acetates may have been a driving force for a shift in pheromone composition. Such tests are necessary to move towards an evolutionary understanding of the differentiation in sexual communication in Heliothis spp. moths.}, number={12}, journal={Journal of Chemical Ecology}, author={Groot, A.T. and Ward, C. and Wang, J. and Pokrzywa, A. and O’Brien, J. and Bennett, J. and Kelly, J. and Santangelo, R.G. and Schal, C. and Gould, F.}, year={2004}, pages={2495–2514} }
 @article{drijfhout_groot_beek_visser_2003, title={Mate location in the green capsid bug, Lygocoris pabulinus}, volume={106}, ISSN={["1570-7458"]}, DOI={10.1046/j.1570-7458.2003.00016.x}, abstractNote={AbstractHeadspace extracts from female Lygocoris pabulinus (L.) (Heteroptera: Miridae) as well as female leg extracts attracted male L. pabulinus in Y‐track olfactometer bioassays. In contrast, only female leg extracts were active in the vibration bioassay. Male extracts had no activity at all in either bioassay. When the female leg extract was analysed by coupled gas chromatography‐electroantennography (Z)‐9‐pentacosene and (Z)‐7‐pentacosene were EAD‐active. (Z)‐9‐Pentacosene and sometimes (Z)‐7‐pentacosene were also observed in female headspace extracts. EAG responses could be obtained for (Z)‐9‐pentacosene. A mixture of (Z)‐9‐pentacosene and (Z)‐7‐pentacosene in the ratio 5 : 1 elicited vibration behaviour in males. The results indicate that these alkenes are important cues for male L. pabulinus in mate location behaviour.}, number={2}, journal={ENTOMOLOGIA EXPERIMENTALIS ET APPLICATA}, author={Drijfhout, FP and Groot, AT and Beek, TA and Visser, JH}, year={2003}, month={Feb}, pages={73–77} }
 @article{groot_heijboer_visser_dicke_2003, title={Oviposition preference of Lygocoris pabulinus (Het., Miridae) in relation to plants and conspecifics}, volume={127}, ISSN={["1439-0418"]}, DOI={10.1046/j.1439-0418.2003.00669.x}, abstractNote={Abstract: To predict possible locations of Lygocoris pabulinus (L) in the field during the summer, we determined their oviposition preference under summer conditions. With L. pabulinus reared on potato, oviposition preference was determined for potato, tomato or green bean. As preference may depend on larval or early adult experience, the oviposition preference of bugs reared on green bean for three generations, and of bugs captured from the field 12 h prior to the experiment was also determined. All females showed a strong preference for potato plants, on which fecundity was higher. Hence, although L. pabulinus is a generalist in its feeding habits, the summer generation seems to be an oviposition specialist. Aggregation of ovipositing females does not seem to occur; similar amounts of eggs were oviposited in plants with clip cages containing conspecifics as in plants without conspecifics. More eggs were oviposited in damaged plants than in undamaged plants. Plant volatiles released upon damage may aid L. pabulinus females in finding suitable oviposition sites.}, number={2}, journal={JOURNAL OF APPLIED ENTOMOLOGY}, author={Groot, AT and Heijboer, A and Visser, JH and Dicke, M}, year={2003}, month={Mar}, pages={65–71} }