Sexual Communication in Diurnal Moths: Behaviors and Mechanisms

International Journal of Tropical Insect Science (2021) 41:15–24 https://doi.org/10.1007/s42690-020-00174-z

MINI-REVIEW

Sexual communication in diurnal moths: behaviors and mechanisms

Lian Chen1 & Xiao-Yun Wang1 & Wen Lu1 & Xia-Lin Zheng1

Received: 17 February 2020 /Accepted: 26 May 2020 / Published online: 1 June 2020 # African Association of Insect Scientists 2020

Abstract Butterflies and moths have substantially different daily activities; butterflies are diurnal, while moths are largely nocturnal or crepuscular. Diurnal moths are subject to different evolutionary pressures that affect several aspects of their behavior and physiology, particularly sexual communication. In this review, species of diurnal moths and the behaviors and mechanisms of their sexual communication are summarized. Diurnal moths are day–flying insects whose partner–finding strategies include visual, olfactory and auditory signals. Males of diurnal Lepidoptera find mating partners using olfactory cues (e.g., sex pheromones) over relatively long distances, or visual (e.g., compound eyes) and/or auditory cues (e.g., ears) over short distances, or even act in combination with the three types of signals. Pheromone–binding proteins and histamine and visual genes play important roles during the signal conduction of sexual communication in diurnal moths. However, the regulatory mechanisms of acoustic communication in day–flying moths are unclear. Understanding this information may help us to explore the evolution of sexual communication in Lepidoptera and to improve biotechnological control strategies against harmful day–flying moths.

Keywords Sexual behaviors . Olfaction . Pheromone–binding proteins . Vision . Visual pigment opsins . Lepidoptera

Introduction commonly deemed as a key signal for recognizing mates in butterflies (see review in Arikawa 2017). The visual system of Lepidoptera is one of the four mega–diverse insect orders and butterflies typically consists of compound eyes (Arikawa the most diverse insect group with currently approximately 2017). Interestingly, the nipple structure on most butterfly 165,000 described species, including butterflies and moths compound eyes has been gradually reduced or even disap- (Kristensen et al. 2007). Butterflies are mainly diurnal, so they peared, so this may be one reason why they are diuristic in- are evolved greater flight abilities, the wings of diurnal species sects. For example, the Papilionidae family is usually only have higher aspect ratios (ARs) and lower wing centroids active under strong light conditions, so its compound eye nip- (WCs) (Penz and Heine 2016). In contrast, moths are mostly ples are shorter or have been absent (Stavenga et al. 2006). nocturnal, and their activities (e.g., emergence, foraging, mat- Visual signals involve polarized light (Sweeney et al. 2003), ing, and oviposition) occur during the night (review in Groot speckle (Jiggins et al. 2001), color (Brunton and Majerus 2014;Chenetal.2018). However, activities of some species 1995; Bybee et al. 2011), and spectral reflectance (Imafuku of moths, such as Castniidae, Phaudidae, Sphingidae, and 2013). However, olfactory signals are used by nocturnal moths Zygaenidae moths (Jo et al. 2014; review in Subchev 2014; (Martin et al. 2011). Olfactory signals are chemical volatiles Monteys et al. 2016; Zheng et al. 2019), are only observed in released by the glands of the male or female adults for the daytime. attracting mates or homologous individuals over short or long Visual and/or olfactory cues mediate the orientation of most distances (Jurenka 2017). For diurnal moths, males likely Lepidoptera adults during mating. Visual communication is search for mating partners through olfactory cues over relatively long distances and use both visual and auditory cues within short distances (Toshova et al. 2007; Kondo et al. * Xia-Lin Zheng 2012; Rowland et al. 2014). Specifically, olfactory cues play [email protected] an essential role in mate recognition, whereas visual and/or

1 auditory cues are of supplementary function (Toshova et al. Guangxi Key Laboratory of Agric-Environment and Agric-Products – Safety, National Demonstration Center for Experimental Plant 2007;DelleVedove et al. 2014; Rowland et al. 2014). Science Education, College of Agriculture, Guangxi University, Therefore, the discovery of the above–mentioned strategies Nanning, China 16 Int J Trop Insect Sci (2021) 41:15–24 of sexual communication in diurnal moths is the key to ex- the family Zygaenidae, including 19 kinds of esters, 2 alde- ploring their evolution in Lepidoptera (Monteys et al. 2016). hydes and 1 alcohol (unpublished data). Most sex attractants In this review, species of diurnal moths and the behaviors showed good attraction effect for male moths in the fields and mechanisms of their sexual communication are summa- suggesting females emitting sex pheromone to attract males rized. The aim is to ascertain the gaps in knowledge about (Subchev 2014). sexual communication in diurnal moths. Visual signals are also important in the sexual communication of diurnal moths. For example, optical cues are used by males of Zygaena trifolii Esper (Lepidoptera: Zygaenidae) Species of diurnal moths during the morning, occasionally leading to ‘morning copulate’ (Hofmann and Kia–Hofmann 2010). Typical short– A total of 14 families of diurnal moths has been recorded, distance approach behaviors such as follow–up flight and ori- including Agaristidae, Arctiidae, Castniidae, Erebidae, ented alight are observed in calling males, providing evidence Geometridae, Gracilariidae, Lymantriidae, Noctuidae, that the sexual communication behavior of male moths is usu- Phaudidae, Sesiidae, Sphingidae, Trydidae, Uraniidae and ally initiated by vision (Seitz and Strand 1913; Zagatti and Zygaenidae (Table 1). At present, most studies of diurnal Renou 1984). Following male approach behavior, a female moths are focused on the species of Sesiidae. Undoubtedly, will either accept or refuse the male’s courtship. At the begin- many species of diurnal moths live on the earth but have not ning of courtship, a male with semi–open wings will walk been reported. Therefore, the species of diurnal moths could around an adjacent female. Both sexes mutually fly, or the represent more than 14 families. male flies with quick fluttering around the female alone after the male locates the female. The male subsequently exposes his aedeagus, trying to copulate. Meanwhile, the female moth bends her abdomen, extending to an angle of 90 degrees from Behaviors of sexual communication in diurnal the ventral surface with an ovipositor and glands. However, moths some females will reject a male by dancing away from the male. A male who is refused, with exposed aedeagus, tries Olfactory signal is one of the important signals of diurnal to copulate again or searches for females near resting sites moth in sexual communication (Uehara et al. 2015, 2016). and repeats searching flight, walking and fluttering. When Both sexes display scent–related behaviors (calling and copulation is established, adults set all of their wings vertical- scratching) after they enter into photophase. First, females ly. These short–distance visual courtship behaviors constitute actively walk or fly around host plants or stay at leaves or aso–called ‘pursuit loop’ that is represented in the behavioral branches. Females grasp the antennae with the foreleg tibias flowchart by a high level of returns from the interaction to the and scrape their antennae in an anterior direction or quiver approach phase (Klein and de Araújo 2010). their abdomens. Second, males perform noteworthy searching Insects use various ways to produce sounds (e.g., rubbing flights and shift their flight directions toward females as they of body parts together and sing), and a tympanic membrane in detect female sex pheromone. Analysis of behavioral transi- the abdomen or in the tibiae of the front legs is mostly used to tions revealed that the male follow–up flight, followed by an detect sound (Baitharu et al. 2018). Although there are many oriented alight, was the only significant sequence leading to explanation for ears in diurnal moths (Fullard and Dawson contact and interaction between males and females for both 1999), increasing empirical studies indicate that the auditory rapid and prolonged courtship sequences. The follow–up signal also play an auxiliary role in the sexual communication flight, which was highly dependent on preceding female of diurnal moths (Conner 1987, 1999;SurlykkeandFullard flight, represented the typical male approach behavior. It can 1989; Sanderford et al. 1998; Surlykke et al. 1998;Nakano be seen that olfactory sensation plays an important role in et al. 2015). For example, Hecatesia spp. males, a diurnal sexual communication of diurnal moths (Kondo et al. 2012). Australian whistling moth, strike the forewings above the Similar to Carmenta Theobromae Busk (Lepidoptera: back to produce sounds, which play a role in agonistic inter- Sesiidae), the calling behavior of females coincided with si- action with males and in female attraction (Bailey 1978). multaneous and more intense flight, walking, or wing However, intraspecific acoustic communication of both sexes fluttering activity in males (Morillo et al. 2009). Currently, in moths usually occurred at close distances (Conner 1999; the sex pheromones of some diurnal moths have been reported Muma and Fullard 2004), such as Lymantria dispar (Matsuoka et al. 2008; Kondo et al. 2012; Yamakawa et al. (Lepidoptera: Erebidae) (Rowland et al. 2014). 2012; Zhang et al. 2012;Subchev2014; Bao and Wang 2015; However, the strategies of sexual communication in diurnal Uehara et al. 2015; Zheng et al. 2019). Among of them, most moths appear to be divergent in different species. Generally, species belongs to the family Zygaenidae (Subchev 2014). So diurnal moths use olfactory and visual signals to identify male far, a total of 22 sex attractants identified from 57 species in and female sexes in some species. This double safeguard Int J Trop Insect Sci (2021) 41:15–24 17

Table 1 Speciesofdiurnalmoths

Family Genus Species References

Agaristidae Phalaenoides P. tristifica Horridge et al. 1977 Arctiidae Amata A. fortunei Kondo et al. 2012 Callimorpha C. quadripunctaria Brakefield and Liebert 1990 Ctenucha C. virginica Sanderford et al. 1998 Cycnia C. tenera Dawson and Fullard 1995 Lycomorpha L. pholus Muma and Fullard 2004 Syntomoides S. imaon Matsuoka et al. 2008 Castniidae Castniid Castniid sp. Quero et al. 2017 Hista H. oiticica Moraes et al. 2010 Paysandisia P. archon Delle–Vedove et al. 2014 Synemon S. plana Cheryl and Attiwill 2010 S. kimberleyensis Braby et al. 2020 Erebidae Amata A. emma Lu et al. 2013 Callistege C. mi Saarinen et al. 2005 Euclidia E. glyphica Saarinen et al. 2005 Parasemia P. plantaginis Rönkä et al. 2018 Polypogon P. tentacularia Valtonen et al. 2006 Geometridae Angerona A. prunaria Valtonen et al. 2006 Aplocera A. praeformata Valtonen et al. 2006 Arctia A. virginalis Grof–Tisza et al. 2017 Archiearis A. parthenias Surlykke et al. 1998 Athroolopha A. latimargo Guerrero et al. 2020 Cabera C. exanthemata Valtonen et al. 2006 Chiasmia C. clathrata Saarinen et al. 2005 Colostygia C. pectinataria Saarinen et al. 2005 Cystidia C. couaggaria Yamakawa et al. 2012 Epirrhoe E. alternata Saarinen et al. 2005 E. tristata Saarinen et al. 2005 Idaea I. pallidata Saarinen et al. 2005 I. serpentata Saarinen et al. 2005 Lythria L. cruentaria Saarinen et al. 2005 Macaria M. brunneata Valtonen et al. 2006 Milionia M. basalis Lin et al. 2017 Odezia O. atrata Saarinen et al. 2005 Siona S. lineata Valtonen et al. 2007 Scopula S. immorata Saarinen et al. 2005 S. floslactata Saarinen et al. 2005 Scotopteryx S. chenopodiata Saarinen et al. 2005 Timandra T. griseata Valtonen et al. 2007 Trichodezia T. albovittata Muma and Fullard 2004 Gracilariidae Lithocolletis L. ringoniella Meng et al. 2010 Lymantriidae Lymantria L. dispar Charlton and Cardé 1990 Orgyia O. ericae Chen et al. 2011 Parocneria P. orienta Zhang et al. 2012 Gynaephora G. alpherakii Bao and Wang 2015 Noctuidae Caenurgina C. rechtea Fullard et al. 1997 Cerapteryx C. graminis Valtonen et al. 2007 Chersotis C. cuprea Valtonen et al. 2006 Cryptocala C. chardinyi Valtonen et al. 2006 Lygephila L. pastinum Valtonen et al. 2007 Teia T. anartoides Shiel et al. 2015 Phaudidae Phauda P. flammans Zheng et al. 2019 Sesiidae Aschistophleps A. argentifasciata Agnieszka et al. 2018 Cephonodes Cephonodes sp. Eguchi 1982 Ichneumoptera I. gryphus Liang and Hsu 2015 Kantipuria K. glansvorax Liang and Hsu 2015 Melittia M. oedipus Reddy et al. 2009 M. bombyliformis Ding et al. 2004 Osminiini Osminiini sp Skowron et al. 2015 Paranthrenella P. dortmundi Liang and Hsu 2015 P. helvola Liang and Hsu 2019 P. weiyui Liang and Hsu 2015 18 Int J Trop Insect Sci (2021) 41:15–24

Table 1 (continued)

Family Genus Species References

Podosesia P. syringae Chouinard et al. 2006 Sesia S. rhynchioides Wang 1990 S. siningensis Yan et al. 2020 S. tibialis Chouinard et al. 2006 Sphecosesia S. litchivora Yang et al. 2008 Synanthedon S. acerni Chouinard et al. 2006 S. acerrubri Chouinard et al. 2006 S. exitiosa Chouinard et al. 2006 S. fulvipes Chouinard et al. 2006 S. castanevora Lu et al. 2009 S. tipuliformis James et al. 2001 S. myopaeformis Eby 2012 S. Pyri Chouinard et al. 2006 S. scitula Chouinard et al. 2006 Synthedon S. Auritinctaoidis Liang and Hsu 2019 S. ceraunuus Liang and Hsu 2015 S. phoenix Liang and Hsu 2015 Sphingidae Euproserpinus E. euterpe Rubinoff et al. 2015 E. phaeton Rubinoff et al. 2015 E. wiesti Rubinoff et al. 2015 Hemaris H. affinis Uehara et al. 2015 H. fuciformis Koshkin and Yevdoshenko 2019 H. ottonis Koshkin and Yevdoshenko 2019 H. radians Koshkin and Yevdoshenko 2019 H. tityus Saarinen et al. 2005 Hyles H. gallii Saarinen et al. 2005 Macroglossum M. koreanum Jo et al. 2014 M. stellatarum Balkenius et al. 2006 Macroglossum sp. Eguchi 1982 Neogurelca N. himachala sangaica Uehara et al. 2016 Thyrididae Rhodoneura R. sphoraria Chen et al. 2002 Uraniidae Lyssa L. zamoa Liang et al. 2016 Urania U. boisduvalii Nunez–Penichet et al. 2019 Zygaenidae Elcysma E. westwoodii Koshio 1996 Histia H. rhodope Yang et al. 2020 Illiberis Illiberis sp. Kim et al. 2004 Soritia S. leptalina Tang et al. 2017 Theresimima T. ampellophaga Toshova et al. 2007 Thyrassia T. penangae He et al. 2017 Zygaena Z. anthyllidis Dieker et al. 2011 Z. exulans Dieker et al. 2011 Z. trifolii Fänger and Naumann 2010 Z. viciae Saarinen et al. 2005

mechanism is of paramount importance to sexual communica- visual signals for sexual communication, e.g., Paysandisia tion. Typically, moths find mating partners using olfactory archon Burmeister (Quero et al. 2017). In some other cases, cues over relatively long distances, while they use visual cues moths could also use chemical and sound signals for sexual over short distances. For example, male Theresimima communication, e.g., Paysandisia archon Burmeister (Quero ampellophaga Bayle–Barelle, 1808 (Lepidoptera: et al. 2017). Furthermore, moths could also use chemical and Zygaenidae) is attracted by a calling female who emits phero- sound signals for sexual communication in other species mones for long range attraction, and then visual cues affect the (Conner 1999; Ryo and Keisuke 2019). Interestingly, the sex- guidance of the flying male in a close range (Toshova et al. ual communication of L. dispar dispar involve chemical, 2007). This phenomenon has been observed in sound and visual signals: (1) males attracted by female sex M. pyrrhostictum (Balkenius et al. 2006), Synanthedon pheromone; (2) males flying toward calling females; and (3) myopaeformis Borkhausen, 1789 (Lepidoptera: Sesiidae) sound signals from flying males at close range inducing move- (Eby 2012)andP. flammans (Unpublished data; Fig. 1). In ment in females, meanwhile, female could orient the males some cases, female lost their gonads so that they primary used used their visual signals (Rowland et al. 2014). Therefore, Int J Trop Insect Sci (2021) 41:15–24 19 the olfactory, visual and auditory signals may be involved sexes, from Phauda flammans (Walker) (Lepidoptera: individually or jointly the sexual communication of diurnal Phaudidae) were identified. PflaPBP1 could bind the female moths depending on the species. sex pheromones Z–9–hexadecenal and (Z, Z, Z)–9, 12, 15– octadecatrienal, while PflaPBP2 could bind only (Z, Z, Z)–9, 12, 15–octadecatrienal (unpublished data). However, the PRs in this species remains unclear. Mechanisms of sexual communication in diurnal moths Visual mechanisms Olfactory mechanisms Light signals induce an insect to produce corresponding be- Pheromone–binding proteins (PBP) and pheromone–receptor havioral responses through the mutual conduction of the re- proteins (PR) are crucial in the process of pheromone– fractor into the visual center. Then, as each ommatidia is a mediated sexual communication (Breer 1997). These proteins complex collection, the slim light with projection lines and could help male moths to detect sex pheromones emitted by gratings in the field of view of the eyes converts the optical females (Holdcraft et al. 2016). The process of perceiving sex signal into an electric signal by crossing of the axons, or neural pheromones in the air by the olfactory sense organs of moths convergence. Finally, with the signal transmitted to the brain, is divided into five steps: (1) the odor molecules enter the the brain integrates and coordinates information from sensory lymph of the sensilla through the wall holes on the epidermis neurons found in the visual system (Leng and Na 2009). of the sense organs; (2) the odorants combine with the PBPs to Visual perception and related morphology, including photore- form a complex; (3) the complex passes through the sensillar ceptors and structural components of compound eyes, are lymph, directly combining with the PRs; (4) the signal trans- highly developed in lepidopteran insects. Butterflies have duction is carried out with the joint involvement of a variety of the typical apposition eyes of diurnal insects that allow them proteins, such as sensory neuron membrane proteins (SNMPs) to adapt better to their lifestyle. It is interesting to note that and odorant–degrading esterases (ODEs), and the signal trans- diurnal moths have bright colors and stripes similar to butter- duction causes the neuron to fire and propagate the action flies. Male will display the bright color on the wings that potential into the antennal lobe and the integration of the sig- facilitate them to be found by females when they attempt to nal into the central nerve to form the command; and (5) after courtship, for example in Paysandisia archon Burmeister, the sensory neuron fires, the odorant molecules are inactivated 1880 (Lepidoptera: Castniidae) (Primo et al. 2018). by a molecular trap that is not yet discovered, and the odorant The histamine is the only neurotransmitter identified in molecules are rapidly degraded by pheromone–degrading en- arthropod photoreceptors (Hardie 1987;Nassel1991; Akashi zyme (PDE) (Stengl 2010). et al. 2018). The synaptic transmission of photoreceptors to The mechanisms of sex pheromone communication of secondary neurons is mediated by the activation of histamine– moths is one of the well studies in animals, especially for gated chloride channel (HCL). These histamine synapses are nocturnal moths (Cardé and Haynes 2004; Allison and also conserved in the visual system of insects. A study pro- Cardž 2016; Groot et al. 2016). However, only a few diurnal vided the first comparative anatomy of histamine–gated chlo- moths had been well studied on the functional role of PBPs ride channels in the vision system of Papilio xuthus Linnaeus, and PRs in sex pheromone detection. For example, recent 1767 (Lepidoptera: Papilionidae) and obtain higher localiza- studies showed that the BmPBP1 plays a crucial role in en- tion resolution than before (Chen et al. 2018). At present, hancing the sensitivity, but not the selectivity, of sex phero- histamine has only been preliminarily studied in Drosophila mone detection in Bombyx mori (L.) (Shiota et al. 2018), and and P. xuthus (Han et al. 2017;Chenetal.2018). It has been odorant receptors 1 of Bombyx mori (BmOR–1) is a G found that the regulatory mechanisms of both protein–coupled sex pheromone receptor that recognizes D. melanogaster and P. xuthus are similar, but they respond bombykol in silk moths (Sakurai et al. 2004). Similar to differently to gamma–aminobutyric acid (GABA). In L. dispar (L.), the gene that encodes the olfactory receptor P. xuthus, medullary neurons not only receive color signals co–receptor (OrCo) were identified and confirmed that it is from histamine, but also receive mixed color and motion sig- critical to odor recognition (Lin et al. 2015). For Manduca nals from large monopolar cells (LMCs), including GABA sexta (L.), the antennal transcriptome was analyzed (Grosse– signals. In contrast, medullary neurons in D. melanogaster Wilde et al. 2011) and PBPs had been detected in male and only receive histamine color signals because they are insensi- female moths (Györgyi et al. 1988), unfortunately, their mech- tive to GABA. Therefore, the differences perhaps appeared anisms of theses PBPs behind remains unclear. Our recent during the early visual processing. Further study the histamine findings showed that two novel PBPs (PflaPBP1 and in diurnal and nocturnal moths may be able to decipher the PflaPBP2), expressed predominantly in the antennae of either evolutionary characteristics of species. 20 Int J Trop Insect Sci (2021) 41:15–24

Fig. 1 Behavioral sequence of mating behavior in male and female Phauda flammans. Yellow arrows indicate female sequences, and blue arrows indicate male behavioral sequences

The visual genes of some Lepidoptera have been cloned of visual genes. These ideals as mentioned above can be ap- but there are few functional reports (Yuan et al. 2010). In plied for the study of diurnal moths, producing insights that butterflies, Kitamoto et al. (1998) described the localization could be helpful to explore the visual evolution of of newly identified visual pigment opsins in the tiered retina of Lepidoptera. P. xuthus. Three cDNAs encoding visual pigment opsins were cloned (i.e., PxRh1, PxRh2 and PxRh3), and then histological Auditory mechanisms in situ hybridization was performed to localize their mRNAs in the retina. The results showed that both PxRh1 and PxRh2, Ultrasonic ears of diurnal moth have also been approved for which are sensitive in the green wavelength region (green conspecific acoustic communication (Sanderford et al. 1998; receptors), correspond to visual pigments and are expressed Fullard and Dawson 1999; Muma and Fullard 2004; in photoreceptor cells, whereas PxRh3 corresponds to a pig- Fernández et al. 2013; Pérez Álvarez and Barro 2014; ment in red receptors (Kitamoto et al. 1998). In nocturnal Rowland et al. 2014;Moraetal.2015). In some cases, the moths, the phototropic opsin gene has been found in some ears undergo dynamic frequency up–tuning during sound species. For example, Ha–UV, Ha–BL and Ha–LW were iden- stimulation, for example in Urania boisduvalii Guérin– tified from Helicoverpa armigera Hübner, 1808 (Lepidoptera: Méneville and Empyreuma pugione (L.) (Mora et al. 2015). Noctuidae) (Yan et al. 2014), and Se–UV, Se–BL and Se–LW However, acoustic communication in the diurnal moths are were identified from Spodoptera exigua Hübner, 1808 still focused on the behavior (Conner 1987; Surlykke and (Lepidoptera: Noctuidae) (Liu et al. 2018). The ultraviolet Fullard 1989;Sanderfordetal.1998;Surlykkeetal.1998; (UV) and blue (B) opsins aided the recognition of short– Fernández et al. 2013; Pérez Álvarez and Barro 2014), and wavelength light during the day, while the long–wavelength the regulatory mechanisms behind are unclear. In some insect (R) opsin might be useful in a dim–light environment. species, male courtship and acoustic communication have Furthermore, the R opsin might aid in locating potential sex been the most heavily studied, resulting in the identification partners and improving mating success over relatively short of dedicated sensory centres, processing circuits and specific distances. For diurnal moths, there have no functional reports motor patterns (Greenfield 2014; Ellendersen and von Int J Trop Insect Sci (2021) 41:15–24 21

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