Sexual Communication in Diurnal Moths: Behaviors and Mechanisms

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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 phero- mones) 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 rela- tively 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 communica- tion 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 copu- late’ (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.
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