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Circadian Rhythms of Sexual Activities in Moths a Review Groot, A.T UvA-DARE (Digital Academic Repository) Circadian rhythms of sexual activities in moths A review Groot, A.T. DOI 10.3389/fevo.2014.00043 Publication date 2014 Document Version Final published version Published in Frontiers in Ecology and Evolution License CC BY Link to publication Citation for published version (APA): Groot, A. T. (2014). Circadian rhythms of sexual activities in moths: A review. Frontiers in Ecology and Evolution, 2, [43]. https://doi.org/10.3389/fevo.2014.00043 General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:01 Oct 2021 REVIEW ARTICLE published: 07 August 2014 ECOLOGY AND EVOLUTION doi: 10.3389/fevo.2014.00043 Circadian rhythms of sexual activities in moths: a review Astrid T. Groot 1,2* 1 Department of Evolutionary Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands 2 Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany Edited by: The circadian rhythm of behavior has interested many researchers in the past decades, Emmanuelle Jacquin-Joly, Institut yet amazingly little is known on the evolution of natural variation in circadian rhythms National de la Recherche of behavior. Most research has been focused on identifying the circadian clock genes Agronomique, France that form an intricate clock network, which turns out to be more complex with every Reviewed by: Monika Stengl, Universität Kassel, discovery. To understand the importance of circadian rhythms of behavior in speciation, Germany genetic analyses should be conducted on intra- and interspecific allochronic differentiation Christine Merlin, Texas A&M of behaviors. Many moth species show specific daily activity rhythms in their sexual University, USA activities, some species being sexually active early at night, while others are sexually *Correspondence: active late at night. This differentiation has been suggested to have arisen to minimize Astrid T. Groot, Department of Evolutionary Biology, Institute for communication interference between closely related species, as co-occurring and closely Biodiversity and Ecosystem related species with overlapping sex pheromone blends show a temporal differentiation Dynamics, University of in their daily sexual activities. However, the genetic differentiation of this allochronic Amsterdam, Science Park 904, separation has barely been examined in any species so far. In this review I summarize 1098 XH Amsterdam, Netherlands e-mail: [email protected] studies conducted on timing of sexual activities in moths, and which factors have been found to influence this timing, with the aim to identify the gaps and challenges, to unravel the possible contribution of allochronic differentiation of sexual activities in moth speciation. Keywords: sexual communication, diurnal rhythm, female pheromone, male response, sex pheromone production INTRODUCTION larger moths and butterflies (Lepidoptera, Apoditrysia), because Virtually all life on earth experiences a 24-h circadian rhythm, natural variation in timing of sexual activity has been found which affects almost all behaviors, including sexual activity and within and between species (see Table 1). The Apoditrysia consist mating. Circadian rhythms are governed by an endogenous cir- of ∼145.000 species, the majority of which (∼120.000) are moths cadian clock: their behavioral patterns are maintained even in (Bazinet et al., 2013), and thus the second most diverse group of the absence of direct cues (Edery, 2000; Sandrelli et al., 2008; insects after the Coleoptera. Bloch et al., 2013). Circadian clocks are entrained by or syn- In moths, reproductive isolation mostly results from species- chronized to the 24 h light/dark cycle by external environmental specific sex pheromone blends (e.g., Roelofs and Carde, 1971; cues, so-called Zeitgebers, such as light and temperature. Timing Roelofs et al., 1974; Cardé et al., 1977; Greenfield and Karandinos, of mating also follows a daily rhythm in many species, which 1979; Greenfield, 1981; Haynes and Birch, 1986; El-Sayed, 2014). can be crucial not only to avoid predators, but also for find- Moth sexual communication seems to be under strong stabiliz- ing the right mating partner, as separation in timing minimizes ing selection, as deviations away from the mean in female signals interference in sexual signaling between species. When species as well as in the male response reduces the chance of finding distributions change due to e.g., global warming or globalization, a mating partner (Miller and Roelofs, 1980; Collins and Cardé, interactions between species with the same timing of activity may 1985; Löfstedt et al., 1990; Cossé et al., 1995; Linn et al., 1997; cause convergence through hybridization or divergence between Zhu et al., 1997; Allison and Carde, 2008). Therefore, the evolu- populations. Thus, separation in timing of mating is a pow- tion of moth sexual communication is an evolutionary mystery erful isolation mechanism among species, and instrumental in (Löfstedt, 1993; Gould et al., 2009). Additional mechanisms that speciation (Tauber et al., 2003; Coyne and Orr, 2004; Devries have been recognized to contribute to species differentiation in et al., 2008; Fergus et al., 2011; Rund et al., 2012). Yet, the role Lepidoptera are habitat isolation (e.g., Roelofs and Carde, 1971; and importance of allochronic differentiation in the evolution Haynes and Birch, 1986; Pashley, 1986), and seasonal and circa- of sexual communication and speciation is almost completely dian variation in female signaling and male response (e.g., Roelofs unknown. and Carde, 1971; Cardé et al., 1975; Teal et al., 1978; Greenfield Speciation through temporal isolation between Drosophila and Karandinos, 1979; Pashley et al., 1992; Monti et al., 1995; species has been linked to circadian clock genes (Kyriacou et al., Sauman and Reppert, 1996; Monti et al., 1997; Froy et al., 2003; 2008), but there is no known naturally occurring dimorphism in Santos et al., 2007, 2011; Zhu et al., 2008; Schöfl et al., 2009; Groot temporal timing of mating activity in fruitflies. The ideal species et al., 2010b; Zhan et al., 2011). However, how these factors may to investigate the importance of timing in speciation are the interact has not been explored systematically. www.frontiersin.org August 2014 | Volume 2 | Article 43 | 1 Frontiers in Ecology and Evolution Groot Table 1 | Timing of sexual activities (sex pheromone titers in female pheromone gland, female calling, male response and mating). Familyily Speciesies Occurrurrencencea Tb L:Dc Time of daye Pherheromonenef Ref g AcActivityd midid mid-lid-late earlrly- Major I II IIIII IV V VIVI °C start S earlrly-midid S mid-lid-late S endend S A midid M componentnent day Pherer Z9 E 12-1414:Ac 1 Noctctuidaeae Spodoptertera exigugua 25 14:10 Callialling Malele 2 | Chemical Ecology Spodoptertera Callialling Z9-1414:Ac 3, 4 26-27 14:10 frugipererda - corn Matiting Noctctuidaeae Spodoptertera Callialling Z 9-1414:Ac 3, 4 26-27 14:10 frugipererda - riceice Matiting Z 9-1414:Ac Spodoptertera Noctctuidaeae 23 12:12 Callialling 5 descescoinsi Z 9E 12-1414:Ac Spodoptertera Noctctuidaeae 23 12:12 Callialling Z 9-1414:Ac 5 latitisfasciacia 25 16:8:8 Pherer Z 9E 11-1414:Ac 6 24 16:8:8 Callialling Callialling– 7 24 16:8:8 pre-exp 25 14:10 Pherer Spodoptertera Noctctuidaeae 25 14:10 Callialling 8 litlittoralislis 25 14:10 Matiting Circadian rhythms of sexual activities in moths 22 17:7:7 Matiting 19 17:7:7 Malele August 2014 | Volume 2 | Article 43 9 Male-le- 19 17:7:7 pre-exp 20 16:8 Calling 10 25 14:10 Calling Z 9E 11-1414:Ac 11 Noctuidae Spodoptera litura 22 16:8 Male 2 18 16:8 Male 10 | 2 (Continued) www.frontiersin.org Table 1 | Continued Groot Familyily Speciesies Occurrurrencencea Tb L:Dc Time of daye Pherheromonenef Ref g AcActivityd midid mid-lid-late earlrly- Major I II IIIII IV V VIVI °C start S earlrly-midid S mid-lid-late S endend S A midid M componentnent day Pher Noctuidae Agrotis ipsilon 25 16:8 Calling Z 7-12:Ac 12 Male 23 D, Noctuidae 17:7 Calling 13 Agrotis segetum 16 N* Z 7-12:Ac 23 17:7 Male 14 26 D, Pher Heliotis virescens 14:10 Z 11-16:Ald 15 24 N Calling 26 D, Pher Heliothis subflexa 14:10 Z 11-16:Ald 16 24 N Calling 25 14:10 Pher em. 17 Helicoverpa zea 26 D, Pher Z 11-16:Ald 16:8 18 20 N Calling Pher Helicoverpa 25 14:10 19 R Calling Z 11-16:Ald armigera 25 16:8 Calling 20 23 15:9 Pher 21 Circadian rhythms of sexual activities in moths 25 16:8 Pher 22 Helicoverpa August 2014 | Volume 2 | Article 43 Noctuidae 25 15:9 Pher Z 9-16:Ald 23 assulta 23 15:9 Calling 21 25 16:8 Calling 22 Pher 24 24 12:12 Calling 25 Noctuidae Trichoplusia ni Male Z 7-12:Ac 26, O** O** Mating 27 | 3 (Continued)
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