# How the diet influences lepidopteran reproduction: Morpho-functional, behavioral, and endocrine aspects

Evan Force, Matthieu Dacher, Stéphane Debernard

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Evan Force, Matthieu Dacher, Stéphane Debernard. How the diet influences lepidopteran reproduction: Morpho-functional, behavioral, and endocrine aspects. Journal of Insect Physiology, 2025, 164, pp.104838. 10.1016/j.jinsphys.2025.104838. hal-05112398

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# How the diet influences lepidopteran reproduction: Morpho-functional, behavioral, and endocrine aspects

Evan Force*, Matthieu Dacher, Stéphane Debernard

Sorbonne Université, Université Paris-Est Créteil, INRAE, CNRS, IRD, Institute for Ecology and Environmental Sciences of Paris, iEES Paris F-75005 Paris, France

## ARTICLE INFO

### Keywords:

- Sexual maturation
- Reproductive system
- Nervous system
- Juvenile hormone
- Insulin signaling pathway
- Fitness

## ABSTRACT

In insects, diet influences the accomplishment of physiological functions, such as reproduction. The study of interactions between diet and reproduction, which involve morpho-functional, behavioral, and endocrine aspects, is necessary for identifying the features of the adaptive strategies of insects in their natural environment. This review delves into the intricate relationship between nutrition and reproductive processes in female and male Lepidoptera. Indeed, nutrient-rich diets are crucial for reproductive success by accelerating ovarian and testicular development, egg maturation, sperm synthesis and migration, and accessory sex gland maturation. Moreover, such diets boost the biosynthesis and release of sex pheromones and promote pheromonal detection by the olfactory system, thus eliciting sexual displays. These physiological and behavioral changes increase fertilization rate and offspring production, highlighting the importance of balanced diets in sustaining insect populations. Then, the review explores the molecular mechanisms by which the evolutionary conserved insulin signaling pathway acts as a transducer of nutritional inputs in linking with the regulatory actions of a major reproductive hormone, namely juvenile hormone. Finally, this review provides a greater comprehensive and integrated understanding of adult diet influence on lepidopteran reproduction, and also opens up new research avenues in the fields of agricultural pest control and ecotoxicology.

## 1. Introduction

Insect physiology is very sensitive to environmental factors that can vary throughout the life of organisms. Indeed, feeding is an environmental factor profoundly influencing their physiology. For instance, *Azteca chartifex* ants exhibited higher thermal tolerances when fed a high-carbohydrate diet and were less tolerant of temperature changes when only water was available (Bujan and Kaspari, 2017); nymphs of the *Schistocerca americana* locust grew into smaller adults and had reduced lipid stores when fed low-nutrient diets, while nymphs raised on high-nutrient diets emerged with larger bodies and greater lipid reserves (Hahn, 2005). This scientific domain has been widely studied in many orders of insects. However, advances in recent years have proven decisive in understanding the close links between diet and reproduction in Lepidoptera, particularly through its influence on the maturation of reproductive systems, the development of sexual behaviors, and the hormonal regulation of these reproductive processes.

Lepidoptera (moths and butterflies) constitute one of the most diverse and abundant animal groups (Kristensen et al., 2007). These

species play a considerable role in the functioning and stability of terrestrial and aquatic ecosystems (Bouchard et al., 2009; Kristensen et al., 2007). Larval and adult stages are closely associated with plants: larvae feed on roots, stems, and/or leaves using their grinding mouthparts (Duan et al., 2022; Jiang et al., 2011), whereas adults often visit flowers to collect nectar by using their proboscis. Floral nectar is mainly composed of water and sugars (sucrose, fructose, and glucose) (Nicolson, 2022; Roy et al., 2017), along with some proteins, amino acids, and lipids following a contamination by pollens (Ares et al., 2018; Lundgren, 2009). Lepidoptera mainly collect nectar rich in sugars, vitamins, and amino acids (Wäckers et al., 2007) essential for their development, flight, and mating (Balzan & Wäckers, 2013; Lavandero et al., 2006; Sun et al., 2021). Moreover, supplementary nutritional resources can promote adult development and improve reproduction (Ellis et al., 2005; Thorpe & Caudle, 1938; Winkler et al., 2006). Many Lepidoptera obtain certain minerals from moist surfaces (Adler, 1982; Beck et al., 1999; Downes, 1973; Ravenscraft & Boggs, 2016). “Puddling” defines a puddle-feeding also including food intakes from various excrement and secretions (from eyes and noses) of living or dead

<footnote>* Corresponding author at: iEES Paris, Sorbonne Université, 4, Place de Jussieu, 75005 Paris, France.</footnote>

<footnote>E-mail address: evan.force@sorbonne-universite.fr (E. Force).</footnote>
animals (Bänziger et al., 2009; Downes, 1973). Puddling behavior does not provide energy but specific micronutrients, such as sodium (Ankola et al., 2021; Boggs & Dau, 2004; Molleman, 2010); and it is exclusive to adults since the low mobility of larvae makes it difficult for them to move toward puddles, and such behavior would expose them to a greater risk of predation. Additionally, puddling behavior is generally observed in male adult Lepidoptera (Molleman, 2010). Furthermore, sodium is involved in excretion as well as locomotion (Dow, 1992; Nicolson, 1976; Peyronnet et al., 2000; Zeiske, 1992), and also has a major role in reproduction by facilitating the sugar absorption in the gut (McLean and Caveney, 1993).

In insects, the mesenteron is the primary site for nutrient assimilation (Li et al., 2021), and glucose is the primary energy source. Glucose is absorbed through the mesenteron's epithelial cells by sodium-glucose co-transporters (SGLTs) and glucose-specific transporters (GLUTs). These transporters are located on the apical and basal membranes of epithelial cells, respectively (Bifano et al., 2010; Caccia et al., 2007; Li et al., 2021). SGLT and GLUT transporters facilitate the transfer of glucose into the hemolymph by the presence of sodium (Bifano et al., 2010). Glucose, a reducing sugar, has osmotic properties that can disrupt insect homeostasis. To maintain low glucose levels in the hemolymph, glucose is converted into a non-reducing sugar, trehalose, in fat bodies (Li et al., 2021). Circulating trehalose is then delivered to cells, where it is hydrolyzed into glucose by membrane-bound and cytosolic trehalases (B. Zhang et al., 2022).

Due to its importance in species propagation and its high potential as a target for pest control, lepidopteran reproduction has been extensively studied, especially in females, and is currently under intense investigation in males. Reproduction occurs once the individual has reached the state of sexual maturity. In both males and females, sexual maturation takes place either during the metamorphosis or early during adult life and mainly results in morphological and functional changes of the reproductive system (Hiroyoshi et al., 2021; Su et al., 2022b; Swevers and Iatrou, 2003; Telfer, 2009). In addition, successful and efficient reproduction relies on the meeting of sexual partners followed by mating (Lees and Zilli, 2019). Meeting sexual partners is a complex process that requires complementary modes of communication between adult males and females. The pheromone-based communication is one of the most used and is generally achieved through the release of sex pheromones by females and the detection of these chemical cues by males (Sarto I Monteys et al., 2016; Tabata, 2018). Furthermore, the onset of sexual behaviors is known to be influenced by endocrine actors, namely biogenic amines (e.g. octopamine and dopamine) and hormones (steroid and sesquiterpenoid hormones) (Force and Debernard, 2025). However, to date, only one hormone with pleiotropic effects is known to be responsible for coordinating sexual behavior development with the maturation of the reproductive system in both adult females and males: the juvenile hormone (JH). For instance, in female moth *Mythimna unipuncta*, JH is involved in the onset of calling behavior and the production of sex pheromones in synchronism with oocyte maturation (Cusson et al., 1994, 1990); and in male moth *Agrotis ipsilon*, JH promotes conjointly the behavioral response to female-emitted sex pheromones and reproductive system maturation (Aguilar et al., 2023; Duportets et al., 1998; Gadenne et al., 1993; Gassias et al., 2021).

This review aims to provide a current state of knowledge on the close connection between adult diet and reproduction in Lepidoptera (with particular emphasis on males for which many advances have recently been discovered) through the compilation of morpho-functional, behavioral, and endocrine (specifically JH, which presents pleiotropic effects on reproduction) studies. Although many aspects of reproduction have been studied in relation to adult diet, there are still many gaps that deserve to be explored in the future, particularly in relation with testicular maturation and spermatogenesis, sex pheromone biosynthesis and female calling behavior, egg-laying, as well as the crosstalk between diet and JH controlling female reproduction. Finally, this review provides a greater comprehensive and integrated understanding of adult

diet influence on lepidopteran reproduction.

## 2. The effect of diet on reproductive system maturation and offspring production

Species sustainability requires the ability of organisms to produce viable offspring. Lepidoptera have internal fertilization and fertilized eggs are laid in protected environments where the young are likely to find food. Embryonic development is supported by lipids, proteins carbohydrates, and also other elements (minerals, vitamins) that are accumulated within maturing oocytes. The synthesis and incorporation of these substances need a lot of energy often acquired through the nutritional intake of females but also by the energy-rich compounds previously stored during the larval stage. Although studied to a lesser extent, male nutritional status is also a determining factor in both reproductive system maturation and the production of spermatozoa.

### 2.1. Diet impacts on morphological and functional changes of reproductive systems

#### 2.1.1. Ovarian development and egg maturation

Typically, the female reproductive system consists in a pair of ovaries each composed of ovarioles, accessory glands, spermatheca, spermatheca gland, medial and lateral oviducts, and bursa copulatrix (Hague et al., 2021). In many species, polytrophic ovaries are thin, transparent, and without eggs in newly emerged adults. With increasing age, ovarioles enlarge and become thicker and more compact. Eggs develop inside the ovary according to asynchronous maturation: eggs located in the lower part of ovarioles mature first (Su et al., 2022b); later, oviducts develop and contain the first mature eggs. Complete maturation of ovaries occurs on average several days after the emergence (Su et al., 2022b). Although egg development and maturation are age-dependent, diet plays a major role in these developmental processes.

He et al. (2021) recently showed that ovary development is directly linked to feeding in *Spodoptera frugiperda* moth. Indeed, sugar-rich nectars supplemented with proteins accelerate the ovarian development compared to fasted females (He et al., 2021). Moreover, a diet composed of sugars (sucrose 20 or 40 % v/v), amino acids (essential and non-essentials), and minerals and vitamins (coming from moist banana) affects the number of eggs inside the ovaries and allows to Lepidoptera females to produce eggs over a longer period (Bauerfeind and Fischer, 2005; Geister et al., 2008; Marchioro and Foerster, 2013). Furthermore, during maturation, eggs increase in size and accumulate water, lipids, proteins as well as sugars (Beenakkers et al., 1985; Cavallini et al., 2023; Diss et al., 1996; García-Barros, 2006; Lee, 2015). It is known that Lepidoptera female diet affects egg maturation: females fed a sugar-only diet lay slightly larger eggs (Bauerfeind & Fischer, 2007) in comparison with eggs coming from females fed with a diet rich in sugars, minerals, and vitamins (Geister et al., 2008). Moreover, during egg maturation, the protein content increases in females fed a sugar-only diet while the lipid amount is invariable. By contrast, the eggs of females fed a diet rich in sugars, minerals, and vitamins accumulate lipids and lose proteins (Geister et al., 2008). Knowing that lipids cover the energy needs for embryonic development and proteins are essential for the formation of structural components like membranes (Beenakkers et al., 1985; Diss et al., 1996), variations in their accumulation during egg maturation suggest that adult female diets would considerably impact embryonic development and affect the viability of offspring.

More broadly in insects, several studies show that development of ovaries is directly linked to feeding in *Drosophila melanogaster* (Diptera), *Paederus fuscipes* (Coleoptera), *Bacon cephi* (Hymenoptera). In these species, nutrients-rich diets (e.g., yeasts rich in proteins for *D. melanogaster*, proteins for *P. fuscipes*, sugars for *B. cephi*) accelerate the ovarian development (Bong et al., 2014; Cavallini et al., 2023; Klepsatel et al., 2020). Moreover, a diet composed of sugars, proteins, minerals, and vitamins affects the number of eggs inside the ovaries (Cavallini
et al., 2023; Huffaker and Gutierrez, 1998) and allows to Coleoptera females to produce eggs over a longer period (Bauerfeind and Fischer, 2005; Rho and Lee, 2016). In parallel with the effects of diet on the maturation of the female reproductive system, recent studies have also demonstrated a considerable diet influence on the male reproductive system.

### 2.1.2. Testicular maturation, spermatogenesis, and sperm bundle migration

In most Lepidoptera males, the reproductive system is composed of two testes producing spermatozoa, two vasa deferens, two seminal vesicles, one ejaculatory duct (or duplex), and two accessory sex glands releasing seminal proteins (Sekhon, 2017). As in females, the male reproductive system is often subject to morphological and functional modifications during adult life (Force et al., 2023; Hiroyoshi et al., 2021). After emergence, adult males undergo remarkable testicular changes characterized by rapid involution (Force et al., 2023; Hiroyoshi et al., 2021). Generally, the latter begins very early in adult life and finishes at the end of sexual maturation. Furthermore, the onset of testicular shrinkage differs between the species. For instance, in male A. ipsilon, this developmental process occurs from the first day to the fifth day of adult life (Force et al., 2023), and is known to be dependent on adult male diet (Force et al., 2023). Indeed, a diet including diversified sugars (sucrose 4% w/w, fructose 4% w/w, and glucose 4% w/w) supplemented with sodium (1% w/w) considerably accelerate the maturation of testes, which is completed in 3 days instead of 5 days for water- and sucrose-fed males (12% sucrose w/w). Testicular shrinkage is probably linked to the completion of spermatogenesis and can also result from the migration of sperm bundles from the testes toward the ejaculatory duct (Chen & Graves, 1970; Hiroyoshi, 2000; Li et al., 2019).

Spermatogenesis is the process by which sperm is produced. As sperm production is energetically costly, diet should have an effect on the number and/or viability of sperm produced. In fact, diet is known to influence sperm production in many insect species (Fedina and Lewis, 2006; Perez-Staples et al., 2008; Perry and Rowe, 2010). However, only a few studies have examined the effects of diet on sperm production in Lepidoptera, such as *Plodia interpunctella* (Gage and Cook, 1994): well-fed males produce more sperm. In the future, it will be very informative to further explore the link between diet and spermatogenesis in Lepidoptera. More broadly in insects, some studies have examined the effects of diet on sperm production, with controversial results. *Bacrocera tryoni* (Diptera) (Perez-Staples et al., 2008), *D. melanogaster* (McGraw et al., 2007), and *Tribolium castaneum* (Coleoptera) (Fedina and Lewis, 2006), produce more sperm when well fed, whereas *Adalia bipunctata* (Coleoptera) (Perry and Rowe, 2010) and *Ceratitis capitata* (Diptera) (Blay and Yuval, 1997) show the opposite pattern. Furthermore, to date, only one study carried out in *Apis mellifera* (Hymenoptera) has examined the effect of feeding on sperm viability, showing that pollen restriction has little effect on sperm viability (Stürup et al., 2013).

Contrary to spermatogenesis, the release of sperm bundles from testes has been studied in several lepidopteran species (Mari et al., 2018; Wergin et al., 1997). Regardless of age, a constant number of sperm bundles leave the testes towards the ejaculatory duct. Interestingly in moths *Spodoptera litura* and A. ipsilon, upon emergence, sperm bundles are already present in the ejaculatory duct (Force et al., 2023; Seth et al., 2016), thus suggesting that the release of sperm bundles occur as early as the pupal stage. Furthermore, during adulthood, sperm bundle transfer is known to depend on diet as in A. ipsilon: migration of sperm bundles occurs in 5 days for fasted and sucrose-fed males (12% w/w), whereas it is finished from the third day of adult life in males fed sucrose (4% w/w), fructose (4% w/w), and glucose (4% w/w) with sodium (1% w/w) (Force et al., 2023). Beyond testicular maturation, spermatogenesis, and sperm migration, the development of male accessory sex glands is also strongly affected by diet.

### 2.1.3. Male accessory sex glands maturation and spermatophore formation

As for testes, during the adult life of males, a significant maturation

of accessory sex glands occurs through morphological modifications (Duportets et al., 1998; Gassias et al., 2021) concomitantly with an increase in seminal protein biosynthesis during the adult life (Duportets et al., 1998; Fernandez and Cruz-Landim, 2005). As described in testes, adult diet of male A. ipsilon affects the accessory sex gland maturation. Indeed, males fed with various sugars (sucrose 4% w/w, fructose 4% w/w, glucose 4% w/w) along with sodium (1% w/w) exhibit higher rates of growth in length and seminal protein than in sucrose-fed males (12% w/w) (Force et al., 2023), as in nutrients-fed males of coleopteran *T. castaneum* (Xu et al., 2015).

Seminal proteins produced by the accessory sex glands are essential for sperm activation by providing nutrients (Gillott, 2003; Happ, 1984) and are involved in the formation of spermatophore (Dorn et al., 1985; Watanabe & Hirota, 1999), a sack containing spermatozoa transmitted to the female during mating (Watanabe and Hirota, 1999). Furthermore, in male butterfly *Papilio xuthus*, spermatophore formation depends on adult diet: 2-day-old virgin males fed sucrose (20%) produce significantly larger spermatophores than those fed water (Watanabe & Hirota, 1999), thus showing the close link between diet and the spermatophore size. In addition, in water-fed males, after mating, the second spermatophore measures approximately half the size of the first and it is heavier due to the increased rest period between two copulations, which is significantly greater than that of the first mating (Watanabe & Hirota, 1999). Besides sugary nutrients, *Manduca sexta* male moths allocate relatively low amounts of nectar-derived amino acids (glycine, leucine, and phenylalanine) to their first spermatophore, but this allocation increases significantly in the second and third spermatophores (Levin et al., 2017). However, in both males and females, the role of amino acids in modulating reproductive system maturation is still far from being understood.

Overall, numerous studies have been carried out on diet effects on morpho-functional modifications of the reproductive system in both female and male Lepidoptera, but other work has focused on offspring production and more broadly on fitness through the study of fecundity (number of fertilized eggs per female), and also hatching of fertilized eggs.

### 2.2. Diet affects fitness by modulating fecundity and hatching

As previously described for reproductive systems, fecundity rate as well as hatching rate are also impacted by adult diet of Lepidoptera. Females fed with rich nutrients (sugars, amino acids, minerals, and vitamins) lay more fertilized eggs compared to starved- or water-fed females (Geister et al., 2008; He et al., 2021, 2022; Su et al., 2022b). Similarly, Force et al. (2024b) show that A. ipsilon males fed with various sugars (sucrose 4% w/w, fructose 4% w/w, glucose 4% w/w) supplemented with sodium (1% w/w) generate a greater number of fertilized eggs than to water-fed males or males fed only with sucrose (12% w/w). Beyond Lepidoptera, in *Callosobruchus maculatus* (Coleoptera), females fed a sugary diet lay on average 20 more fertilized eggs than those not fed or simply fed water (Fox & Moya-Laraño, 2009).

Furthermore, the hatching rate is also linked to adult diet in Lepidoptera. Females fed with sugars (sucrose 20% v/v), minerals and vitamins (from moist banana), lay an increased proportion of hatched eggs in comparison to water-fed females (Geister et al., 2008; He et al., 2021). This same result is observed in A. ipsilon males fed with sucrose (4% w/w), fructose (4% w/w), glucose (4% w/w), and sodium (1% w/w) in comparison to males fed water or sucrose (12% w/w) (Force et al., 2024b). As in Lepidoptera, in *D. melanogaster*, females and males fed with yeast (protein intake) produce 10 times more offspring than individuals fed without yeast (Winkler & Janicke, 2022).

While the role of nectar amino acids in reproductive system maturation is unknown, the involvement of amino acids in lepidopteran fitness has long been a subject of research interest. However, experimental findings regarding the effect of adult-derived amino acids on lepidopterans are often contradictory. For instance, while some species
of butterflies and moths showed no marked positive effect on fecundity (Hill, 1989; O'Brien et al., 2000; Romeis and Wäckers, 2002), other studies revealed that adults fed with amino acid nectar laid more eggs than females fed only sugar nectar (Mevi-Schutz and Erhardt, 2005). Then, in *Coenonympha pamphilus* butterfly, adult females receiving nectar amino acids produced heavier larvae and increased hatching success (Cahenzli and Erhardt, 2012), and males of this species benefited from improved reproduction (Cahenzli and Erhardt, 2013). Despite these findings, the metabolic use and allocation of amino acids by butterflies and moths remain unresolved.

In summary, although the energetic and metabolic aspects are not known, female adult diets rich in nutrients promote ovarian development and egg maturation. Besides, in adult males, the nutrient-rich diets significantly accelerate testes maturation and the migration of sperm bundles from the testes to the ejaculatory duct concomitantly to the development of accessory sex glands and the increase in seminal protein biosynthesis, which causes the production of larger spermatophores. Furthermore, diet impacts on reproductive systems in both female and male Lepidoptera are accompanied by an increase in their fitness: a nutrient-rich diet generates more fertilized eggs and produces more larvae. Following morpho-functional changes in the reproductive systems, individuals reach sexual maturity. This is followed by the display of sexual behaviors that allow for the rapprochement of partners. Just as with the maturation of the reproductive systems, the development of sexual behaviors is also modulated by the adult's diet in Lepidoptera.

### 3. From sexual partner meeting to mating: Diet acts on reproductive behaviors

In Lepidoptera, reproduction involves the meeting of sexual partners followed by mating (Lees and Zilli, 2019). Environmental factors such as diet are important modulators of searching for sexual partners, notably by acting on chemical communication between females and males (Sarto I Monteys et al., 2016; Tabata, 2018).

#### 3.1. Sex pheromone biosynthesis and female calling behavior

Thanks to exocrine glands (commonly referred to as pheromone glands) composed primarily by a single epidermal layer located in various parts of body (Foster and Anderson, 2020; Jurenka, 2003, 2021), adult lepidopteran females release sex pheromones produced from diverse biomolecules (Foster and Anderson, 2020; Jurenka, 2003, 2021). They can synthesize a wide range of pheromonal components (Jurenka, 2003; Roelofs & Bjostad, 1984), either unique or in combination of compounds highly specific to each species (Linn & Roelofs, 1995). Furthermore, adult diet is known to influence the sex pheromone biosynthesis: sugar-rich diets (sucrose or glucose 10 % w/w) promotes the production of sex pheromones (Foster and Anderson, 2015; Foster and Johnson, 2010; Y. Zhang et al., 2020). In other insects, the production of sex pheromones is also influenced by diet as in male *B. dorsalis* (Diptera) with a protein intake from a yeast-based diet (Gui et al., 2023).

Sex pheromone emission occurs during a calling behavior, which is characterized by a lifting of the abdomen favoring the pheromone dispersion. To date, few works focused on the environmental factors controlling such a sexual behavior, but Y. Zhang et al., (2020) indirectly highlighted diet effects on calling behavior in female moth *Mythmina separata*: compared to water-fed females, those fed with sugar (5 %) attracted more males. Knowing that the diet of female *M. separata* impacts the sex pheromone biosynthesis, it is possible to believe that diet could also have a significant effect on sex pheromone release through modulation of calling behavior. Therefore, in the future, it would be interesting to clarify this point. Beyond Lepidoptera, in *Nicrophorus vespilloides* (Coleoptera), Richardson and Smiseth (2019) found that male calling behavior was influenced by its nutritional status. Indeed, males that had been starved during sexual maturation spent more time

practicing calling behavior compared to males fed with a nutrient-rich diet.

#### 3.2. Sex pheromone detection and male behavioral attraction

When exposed to female sex pheromones, the induced behavioral response of the lepidopteran male leading to the rapprochement of the sexes relies on the existence of peripheral and central olfactory structures. As many animal species, insects, and more particularly Lepidoptera, have developed a sophisticated olfactory system allowing them to display their sexual behaviors.

##### 3.2.1. Male peripheral nervous system and detection of female sex pheromones

Male antennae detect female sex pheromones through specific olfactory neurons (Phe-ORNs) (Gadenne et al., 2016; Hansson & Anton, 2000; Hoffmann et al., 2020; Renou et al., 2015) located within the specific olfactory sensilla (Keil, 1999). There, pheromonal molecules bind to olfactory receptors (ORs) placed on the membrane of Phe-ORN dendrites (Gadenne et al., 2016; Hoffman et al., 2020; Renou et al., 2015). To date, ORs have been very well studied in Drosophila (Gomez-Diaz et al., 2018; Masse et al., 2009; Vosshall, 2000) and are highly conserved among all insects (Missbach et al., 2014; Zhao & McBride, 2020). Additionally, Phe-ORNs are very specific and only respond to a few similar molecules or even to a single pheromonal compound (Todd & Baker, 1999). For instance, in male *A. ipsilon*, *AipsOR3* is strongly expressed in antennae (Gu et al., 2014) and is specific for (Z)7-12:Ac pheromonal molecule (Vandroux et al., 2022).

Recently, and for the first time in insects, a link has been established between adult diet and sex pheromone detection in male *A. ipsilon* (*Force et al.*, 2025). Sex pheromone sensitivity is impacted by adult diet: males fed various sugars (sucrose 4 % w/w, fructose 4 % w/w, glucose 4 % w/w) supplemented with sodium (1 % w/w) have a sex pheromone sensitivity threshold around 10 ng, while it is equal to 100 ng for males fed water (*Force et al.*, 2025). In addition, the authors have also demonstrated a diet effect on the Phe-ORNs' response to 10 ng of (Z) 7-12:Ac pheromonal compound (Fig. 1). Indeed, in males fed with various sugars along with sodium, stimulation of Phe-ORNs by (Z)7-12: Ac causes a significant increase in action potential frequency compared to water-fed males (*Force et al.*, 2025). Once recognized by Phe-ORNs, the pheromonal signal is integrated in the primary and secondary olfactory centers, triggering the sex pheromone-mediated behavioral response.

##### 3.2.2. Central nervous system and male associated behavioral response to female sex pheromones

Action potentials emitted by Phe-ORNs reach the primary olfactory center, namely the antennal lobe (AL), which is composed of glomeruli involved in the onset of the integration of pheromonal information, followed by more central brain areas (Greiner et al., 2004; Hansson and Anton, 2000). This integration results in the activation of descending motor neurons, eliciting an appropriated behavioral response. The latter has been very well studied in Lepidoptera, in which males perform stereotypical-oriented flight in response to female sex pheromones (Bau & Cardé, 2015; Cardé & Willis, 2008; Golov et al., 2021; Kennedy, 1983; Liberzon et al., 2018; Mafra-Neto & Cardé, 1994). In the wild, males typically practice random planar flights during which their sensilla collect olfactive stimuli. When female sex pheromones are detected, males face the wind and stop their random flight to move toward the pheromonal source. To avoid losing sex pheromones during oriented flight (Martinez et al., 2013), males adopt a zigzag trajectory becoming less and less ample as they approach the pheromonal source (Baker et al., 1985; Kennedy, 1983). Recent work carried out in male *A. ipsilon* has demonstrated that this oriented flight in response to optimal dose of female sex pheromones is surprisingly unaffected by diet (*Force et al.*, 2024c), although sugar-rich diets improve global flight capacities in
<figure><img src="image_3.png" /><figcaption>**Fig. 1.** Adult diet effects on the detection of female sex pheromones in male Agrotis ipsilon (from Force et al. (2025)). Compared to 5-day-old fasting males, a various sugar diet added with sodium increases pheromonal neuron (Phe-ORN) response to a compound of female sex pheromones ((Z)7-12:Ac). Thus, the specific diet decreases the sensitivity threshold to female sex pheromones in male moths. Figure created in BioRender.com. BL: basal lamina; CU: cuticle; GL: glia cell; HL: hemolymph; P: pore; SL: sensillum lymph; TE: thecogen cell; TO: tormogen cell; TR: trichogen cell.</figcaption></figure>

both males and females Lepidoptera (He et al., 2021; Shirai, 2006; Su et al., 2022b).

Additionally, in male *A. ipsilon*, studies reported an age-dependent increase in the behavioral response to female sex pheromones, from the emergence to the fifth day of adult life, in sucrose-fed males (20 % w/w) (Anton et al., 2007; Gadenne et al., 1993). This increase in behavioral responsiveness is paralleled with a raise in the sensitivity of sex pheromone-responding AL neurons (Anton & Gadenne, 1999). Recent work demonstrated in male *A. ipsilon* that this age-related plasticity of pheromonal system is influenced by diet (Force et al., 2024c). Males fed with various sugars (sucrose 4 % w/w, fructose 4 % w/w, glucose 4 % w/w) along with sodium (1 % w/w) perform an oriented flight from the third day post-emergence whereas males fed only with sucrose (12 % w/w) accomplish this behavioral response only from the fifth day of adult life, thus demonstrating an acceleration in the initiation of oriented flight probably through an early maturation of ALs (Force et al., 2024c). Although the effects of diet on the maturation of primary olfactory centers remain to be explored in lepidopteran males, the relationship between diet and AL neuron response to sex pheromonal compound has been shown in female *D. melanogaster* (Lebreton et al., 2015): in response to the pheromone 11-cis-vaccenyl acetate (cVA), the activity of ventromedial 2 (VM2) glomerulus increases in fed females compared to starved-females. In short, the sex pheromone-mediated behavioral responses allow the rapprochement of sexual partners over long distances. Once in proximity, sexual partners meet and generally display courtship behavior.

### 3.3. Courtship display and mating

Following the rapprochement of sexual partners, several male Lepidoptera perform courtship displays, often characterized by a flight circling females (Barrer and Hill, 1977; Pliske, 1975; Rutowski et al., 2010). To date, it is well known that courtship behaviors are closely related to the nutritional status of organisms, as in butterfly *Battus philenor*: males fed with sodium (0.1 M) take longer to circle females, tend to spend more time courting females before mating, and court females with more vigor than water-fed males (Mitra et al., 2016). Although sodium does not appear to impact the oriented flight performance in some Lepidoptera males (Force et al., 2024c), it plays a role in

courtship flight (Mitra et al., 2016). In addition, sodium intake affects mating success without acting on fertility (Ankola et al., 2021). Taken together, these results suggest that sodium could be an indirect indicator to females reflecting the male's ability to perform efficient mating. Then, knowing that sodium is important to lepidopteran reproduction by improving nutrient absorption (Force et al., 2023, 2024c), this indirect indicator could also reflect the male's ability to generate viable offspring, which would be selected by females. Therefore, it would be very informative in the future to study the sodium-related effects on reproductive physiology as well as sexual behaviors of male Lepidoptera. As in Lepidoptera, it is well known that courtship behaviors are closely related to the nutritional status of insects, as in *Requena verticalis* (Orthoptera) (Schatral, 1993) and *D. melanogaster* (Schultzhaus et al., 2018). For instance, in *D. melanogaster*, females and males fed with sugars and proteins perform courtship display faster than individuals fed with a high-fat diet, resulting in a greater reproductive success (Schultzhaus et al., 2018).

Mating follows a series of behaviors between sexual partners and leads to the transfer of spermatophore from male to female (Hague et al., 2021). The male inserts his aedeagus through the female's copulatory opening and deposits the spermatophore in the bursa copulatrix. Actually, several works demonstrate the diet effect on the mating success in Lepidoptera. In *M. separata* females fed sugar have a mating rate equal to 60 % while it is only 15 % for water-fed females (Zhang et al., 2020). Besides, the diet of male *P. xuthus* affects the mating duration, particularly during a second mating: the duration of copulation is 20 min longer for males fed with sucrose (20 %) than for water-fed males (Watanabe & Hirota, 1999). This increase in copulation duration is correlated with mating success since males fed sugar have a mating success of 70 % instead of 20 % for water-fed males (Watanabe & Hirota, 1999). More broadly in insects, it is well-known that adult diet significantly affects mating success, such as in *D. melanogaster*, for which mating success decreases in females fed with a high-fat diet compared to females fed with sugars and proteins (Schultzhaus et al., 2018); or in *N. vespilloides*, where the nutritional status of females affects the choice of sexual partner and consequently the mating success (Richardson & Smiseth, 2019). Indeed, starved females prefer males fed with a nutrient-rich diet to starved males, while well-fed females have no preference for males (Richardson & Smiseth, 2019). Furthermore, while the diet impacts on
egg-laying are still unknown in Lepidoptera, some studies shed light on the putative influence of nutrient resources in egg-laying in bees (Dolasevic et al., 2020; Donkersley et al., 2014; Pattamayutanon et al., 2018; St. Clair et al., 2022). In the future, it will be of great interest to elucidate the effects of feeding on lepidopteran egg-laying.

To sum up, it is well established that adult diet modulates sexual behaviors in both female and male Lepidoptera although the energetic and metabolic aspects are not known. Indeed, nutrient-diversified diets increase the female sex pheromone biosynthesis and could improve their release by modulating calling behavior. These same regimens promote the detection of sex pheromones by increasing the Phe-ORN sensitivity in males. In addition to diet effects on peripheral olfactory system, nutrient-diversified diets also affect the central nervous system by triggering adapted behavioral responses, such as male-oriented flight toward female sex pheromones. Once sexual partners are close, a diet diversified in nutrients plays a role in courtship display by probably providing energy. This increases the time and the vigor of the court, thus revealing that diet is crucial for mating success.

Although it is highly likely that the effects of diet on reproduction are directly related to the energy intake and metabolic state of individuals, the development and modulation of reproductive behaviors as well as the maturation of the reproductive system in female and male Lepidoptera are, however, well known to be regulated by the endocrine system, and particularly by juvenile hormone for which recent results prove its mediating role in the diet-induced modulation of Lepidoptera reproduction.

## 4. Juvenile hormone: A molecular actor at the interplay between diet and reproduction

In Lepidoptera, juvenile hormone (JH) is involved in the synchrony between sexual behaviors and reproductive physiology in both adult females and males. For instance, in *M. unipuncta* females, JH promotes calling behavior and the sex pheromones biosynthesis, concomitantly with its stimulatory action on oocyte maturation (Cusson et al., 1994, 1990); in males *A. ipsilon*, it is required for the acquisition of sex pheromone responsiveness and the maturation of accessory sex glands (Duportets et al., 1998; Gadenne et al., 1993; Gassias et al., 2021). Knowing that developmental processes linked to reproduction require considerable energetic investment (Su et al., 2022a; B. Zhang et al., 2022), JH has been presumed to mediate the effects of adult diet on the lepidopteran reproductive physiology.

### 4.1. Diet and modulation of juvenile hormone actions

JH is a lipophilic molecule produced and released into hemolymph by the *corpora allata* (CAs), a pair of endocrine glands connected to the brain (Noriega, 2014), and is known to modulate the reproductive physiology in some Lepidoptera (Cheng et al., 2023; Cusson et al., 1990; Duportets et al., 1998; Gassias et al., 2021). Most JH actions are mediated by a nuclear protein complex composed of two members of the basic helix-loop-helix (bHLH)/Per-ARNT-Sim (PAS) transcription factor family: Methoprene-tolerant (Met) (Aguilar et al., 2023; Daimon et al., 2015; Derks et al., 2015; Gassias et al., 2021; Jiang et al., 2011; Miao et al., 2020) and Taiman (Tai) (Lozano et al., 2014; Smykal et al., 2014). Associated with JH, Met-Tai heterodimeric complex binds to an E-box response element in the promoter regions of JH target genes regulating their transcriptional activities (Li et al., 2014, 2011; Zhang et al., 2011). This is the case for *Krüppel homolog 1* (*Kr-h1*), encoding a $C_2H_2$ zinc finger-like transcription factor, known to be an early JH response gene (that functions downstream of the Met-Tai complex) (Aguilar et al., 2023; Kayukawa et al., 2012).

### 4.1.1. *Diet impacts on juvenile hormone actions in regulating reproductive physiology*

JH plays a major role in the reproductive system maturation of

Lepidoptera. An increase in circulating JH level is correlated with ovarian development and oocyte maturation in females (Cusson et al., 1990; L. Zhang et al., 2020), and with development of accessory sex glands concomitantly to an increase in seminal protein production in males (Duportets et al., 1998; Gassias et al., 2021). Moreover, JH signaling involved in reproductive system maturation is well-known (Gassias et al., 2021; Ma et al., 2018; Zhang et al., 2019, 2018). Indeed, *Met* and *Kr-h1* are strongly expressed in ovaries, oocyte membrane (Ma et al., 2018; Zhang et al., 2019, 2018), male accessory sex glands (Gassias et al., 2021), but to a lesser extent in testes (Ma et al., 2018; Zhang et al., 2018). Injections of *Met-* and *Kr-h1*-dsRNA in newly emerged Lepidoptera induce delayed ovarian and oocyte development, decreased eggs laid, impaired male accessory sex gland maturation, and reduced seminal protein synthesis, thus confirming the involvement of the JH signaling pathway in the maturation of female and male reproductive systems (Gassias et al., 2021; Ma et al., 2018; Zhang et al., 2019, 2018). Although the diet effect on JH signaling involved in female reproduction is not elucidated, very recently, a study shed light on the diet effects on the JH pathway within male reproductive organs (Fig. 2A) (Force et al., 2024a). Indeed, a diet diversified in various sugars (sucrose 4 % w/w, fructose 4 % w/w, glucose 4 % w/w) plus sodium (1 % w/w) potentializes the biological actions of JH on accessory sex glands by drastically increasing the expression levels of *Met1*, *Tai*, and *Kr-h1* compared to water-fed males (Fig. 2A) (Force et al., 2024a).

### 4.1.2. Juvenile hormone actions on reproductive behaviors and its modulations by diet

Conjointly with its actions on reproductive systems, JH is also involved in the display of sexual behaviors (Cusson et al., 1994; Force and Debernard, 2025). For example, the calling behavior is correlated with a high circulating JH level in young virgin females *M. unipuncta* (Cusson et al., 1990); application of JH analog, Methoprene, in *M. separata* females increase the mating rate (L. Zhang et al., 2020). Moreover, ablation of CAs in newly emerged males *A. ipsilon* considerably reduces the AL neuron response to the female sex pheromones (Anton & Gadenne, 1999), whereas JH injection in the allatectomized males restores the pheromonal response (Anton & Gadenne, 1999). The involvement of JH in the development of reproductive behaviors results in the activation of the JH signaling pathway within the nervous system. In fact, in adult female moth *Grapholita molesta* and *Helicoverpa armigera*, *Met* and *Kr-h1* are highly expressed in the brain (Zhang et al., 2019, 2018), as in ALs of adult male *A. ipsilon* (Aguilar et al., 2023; Duportets et al., 2012). Furthermore, *Met-* and *Kr-h1*-dsRNA injections in newly emerged males of *A. ipsilon* lead to a decrease in both the expression of JH signaling actors within ALs and the behavioral response to female sex pheromones, thus demonstrating the role of JH signaling pathway in the central processing of sex pheromone signals (Aguilar et al., 2023). Very recently, a study reveals the effect of diet on the JH signaling pathway in the ALs of *A. ipsilon* males (Fig. 2B) (Force et al., 2024a). In comparison with males fed water, males fed various sugars (sucrose 4 % w/w, fructose 4 % w/w, glucose 4 % w/w) and sodium (1 % w/w) strongly expressed *Met1*, *Tai*, and *Kr-h1* in ALs (Fig. 2B) (Force et al., 2024a), probably causing early onset of oriented flight towards female sex pheromones following an induction of the maturation of ALs in this species. Unlike males, the diet effect on reproductive behaviors through the involvement of JH signaling is not yet known in females.

The display of certain sexual behaviors requires the detection of sensory signals, such as during the male-oriented flight towards the female sex pheromone. This behavioral response is only possible if males detect the sex pheromones thanks to their antennae. Furthermore, a recent study shows the presence of JH receptor Met1 within the antennae of *A. ipsilon* males (Force et al., 2025). As at the central level previously described, diet also acts on the peripheral olfactory system through a modulation of the JH receptor in antennae: a diet diversified in sucrose (4 % w/w), fructose (4 % w/w), glucose (4 % w/w) with
<figure><img src="image_4.png" /><figcaption>**Fig. 2.** Adult diet impacts JH signaling pathway actors in accessory sex glands (A), antennal lobes (B), and antennae (C) of Agrotis ipsilon males (from Force et al. (2025, 2024a)). A sugar-rich diet significantly increases the expression of Met, Tai, and Kr-h1 in comparison to water-fed males. Thus, diet affects the JH actions involved in reproduction of male moths. Figure created in BioRender.com.</figcaption></figure>

sodium (1 % w/w) provokes an upregulation of *Met1* gene compared to water-fed males (Fig. 2C) (Force et al., 2025). In parallel with the action on the JH receptor, a diet composed of various sugars with sodium leads to an increase in the expression of *AipsOR3*, an OR involved in the detection of the major pheromonal compound (Z)7-12:Ac released by females (Force et al., 2025). Thereafter, a topical application of Pre-cocene (a molecule degrading the CAs producing JH (Pratt et al., 1980; Pratt & Bowers, 1977)) in male moths fed with this diet cancels its ef-fects and causes a reduction in the expression of JH receptor *Met1*, concomitantly to the inhibition of the expression of *AipsOR3* (Force et al., 2025). These results thus demonstrate the close interplay between diet and the modulation of female sex pheromone detection in male *A. ipsilon* through the JH action (Force et al., 2025).

Consequently, JH acts centrally by modulating the maturation of ALs within the brain, and peripherally by regulating the expression of some specific ORs involved in sex pheromonal communication. To date, diet is well-known to be an external factor regulating the pleiotropic actions of JH in the onset and display of sexual behaviors mainly in male Lepidoptera, but also in other insect orders such as Diptera (Lebreton et al., 2015).

Knowing that activation of JH signaling pathway is dependent on local concentration of the hormone, it was reasonable to believe that diet may modulate JH biosynthesis by CAs. Indeed, JH biosynthesis is known to depend on diet in several insects (Bai et al., 2022; Force et al., 2024a; Leyria et al., 2022; Perez-Hedo et al., 2014). More particularly in Lepidoptera such as male *A. ipsilon*, a diet composed of sugars (sucrose 4 % w/w, fructose 4 % w/w, glucose 4 % w/w) plus sodium (1 % w/w) drastically accelerates and increases the *in vitro* JH biosynthesis by CAs compared to water-fed males, finally leading to a higher circulating JH titer (Force et al., 2024a). Furthermore, several studies performed in different insect species brought in evidence that the insulin signaling pathway acts on the biosynthetic activity of CAs by modulating the expression of the JH biosynthetic enzymes (Abrisqueta et al., 2014; Pan

et al., 2022; Pérez-Hedo et al., 2013; Tu et al., 2005; Zhu et al., 2020). Therefore, this signaling pathway could be involved in the transduction of nutritional signals leading to the regulation of JH biosynthesis in Lepidoptera.

## 4.2. Insulin signaling pathway: A nutritional transducer regulating juvenile hormone biosynthesis

The insulin signaling pathway (ISP) including insulin-like peptides (ILPs) and their receptors (InRs) is highly conserved during evolution and is known to connect food and reproduction by controlling JH biosynthesis in insects (Badisco et al., 2013; Jindra et al., 2013; Noriega, 2014; Smykal & Raikhel, 2015). For instance in *Bombyx mori* moth, the glucose availability favors ILP production by the brain (Masumura et al., 2000). A recent study quantified the expression level of three ILPs (*ILP1*, *ILP2*, and *ILP4*) in the adult brain of *A. ipsilon* males subjected to different diets (Force et al., 2024a). Although the *ILP2* expression is invariant according to diet, males fed a sugary diet (sucrose 4 % w/w, fructose 4 % w/w, glucose 4 % w/w) supplemented with sodium (1 % w/w) express *ILP1* and *ILP4* approximately two times higher than males fed with water (Force et al., 2024a). Furthermore, this same study highlights a connection between diet and JH biosynthesis by assessing (i) the effects on the expression of a key biosynthetic enzyme of JH, namely *HMG-CoA reductase (HMGR)*, and (ii) the *in vitro* JH biosynthesis by CAs, either after an injection of exogenous insulin into 1-day-old males fed with water or after an injection of dsRNA targeting *InR* into 1-day-old males fed with sugars (sucrose 4 % w/w, fructose 4 % w/w, glucose 4 % w/w) plus sodium (1 % w/w). These experiments show that ISP upregulates the expression of *HMGR* in CAs and the JH biosynthesis by CAs (Force et al., 2024c), thus revealing the interplay between food, insulin, and JH biosynthesis in male Lepidoptera (Fig. 3). To date, a significant scientific gap remains regarding the crosstalk between diet, insulin signaling pathway, and JH in Lepidoptera females.
<figure><img src="image_5.png" /><figcaption>**Fig. 3.** Adult diet impacts the juvenile hormone (JH) biosynthesis through the insulin signaling pathway (ISP) in male Agrotis ipsilon (from Force et al. (2024a)). In vitro JH biosynthesis by CAs is significantly increased after an injection of exogenous insulin into 1-day-old males fed with water and drastically decreases after an injection of dsRNA targeting InR into 1-day-old males fed with sugars plus sodium. Thus, diet affects the ISP involved in JH biosynthesis in male moths. Figure created in BioRender.com. CAs: corpora allata; CCs: corpora cardiaca; HMGR: HMG-CoA reductase; ILPs: insulin-like-peptides; InR: insulin receptor; MNSCs: median neurosecretory cells.</figcaption></figure>

In summary, JH is a molecular actor at the interface between feeding and reproduction in male Lepidoptera; and such a transducing role of JH remains to be proven in females. Indeed, diet modulates JH actions on both the reproductive systems and the nervous system involved in the realization of male reproductive behaviors. Modulations on JH actions is a consequence of the diet regulation of its biosynthesis by CAs. This process directly depends on a highly conserved signaling pathway in animals, the ISP, which acts as a nutritional transducer in male Lepidoptera.

**5. Conclusions and future perspectives**

Diet of adult Lepidoptera plays a critical role in shaping both the morphological and functional aspects of their reproductive systems, ultimately influencing their reproductive success and fitness (Fig. 4). For females, nutrient-rich diets significantly enhance ovarian development and egg maturation, while in males, similar diets accelerate testicular maturation, sperm bundle migration, and the development of accessory sex glands. These physiological changes lead to the production of more fertilized eggs and more abundant offspring. Thus, a balanced and nutrient-rich diet is essential for maximizing reproductive potential and ensuring the sustainability of insect populations. This review also highlights the significant role of adult diet in modulating reproductive

behaviors in Lepidoptera (Fig. 4). Nutrient-rich diets increase the sex pheromone biosynthesis and potentially enhance their release in females. These diets also improve the detection of female sex pheromones by the peripheral olfactory system and affect the central nervous system responsible for the integration of sex pheromonal information in males, thus leading to adapted behavioral responses. Moreover, a diet rich in nutrients positively impacts courtship displays and mating success. These findings underscore the importance of diet in lepidopteran reproduction, suggesting that dietary factors are critical for reproductive success and species propagation. We then demonstrate the intricate relationship between diet, JH biosynthesis, and the subsequent effects on reproductive physiology and sexual behaviors in male Lepidoptera exclusively (Fig. 4) because no study has addressed these aspects in males to date. JH serves as a crucial hormonal signal that links nutritional inputs to the reproductive system's development and function, particularly through the ISP. Additionally, diet influences JH biosynthesis and also modulates its actions on central and peripheral olfactory systems, thereby impacting male reproductive behaviors. Thus, we highlight the crucial role of diet in regulating JH signaling pathway that is essential for reproductive success in male Lepidoptera (Fig. 4). Although many aspects of reproduction have been studied in relation to adult diet, there are still many gaps that deserve to be explored in the future, particularly in relation with testicular maturation and
<figure><img src="image_6.png" /><figcaption>Fig. 4. Diet shapes lepidopteran reproduction at the morphological, behavioral, endocrine levels.</figcaption></figure>

spermatogenesis, sex pheromone biosynthesis and female calling behavior, egg-laying, as well as the crosstalk between diet and JH controlling female reproduction.

Due to the high degree of similarity of insulin and lipophilic hormone (such as JH) signaling pathways in animals, including receptor proteins and their downstream participating elements, our review offers the opportunity to extend the understanding of the effects of diet on reproductive physiology to other taxa in Metazoan, particularly through the functional relationships between the nutritional signals and hormonal regulation of reproduction. Furthermore, this has potential applications in agricultural pest management and insect ecotoxicology. In fact, many insect species play a central role in ecosystems as pollinators, although the larvae, often crop pests such as in *Agrotis ipsilon*, can have negative impacts on agriculture (Donahue, 1995; MacGregor et al., 2015). Because they are taxonomically diverse, present in many habitats, and extremely sensitive to human-modified abiotic conditions, Lepidoptera are particularly useful as bioindicators of ecosystem health (Chowdhury et al., 2023; Maleque et al., 2009). Finally, due to the crucial role of the ISP in lepidopteran sexual maturation, our review projects InRs as potential targets for CRISPR-based gene drive technology, which is highly effective against nocturnal pests for instance (Chen et al., 2018; Koutroumpa et al., 2016), and for the development of novel control strategies (X. Zhang et al., 2022). Furthermore, ILPs could be used as molecular biomarkers for monitoring and assessing the impact of

environmental xenobiotic contaminants on the reproduction of pollinators and other economically important insects.

### CRediT authorship contribution statement

**Evan Force:** Writing – review & editing, Writing – original draft, Validation, Supervision, Investigation, Conceptualization. **Matthieu Dacher:** Writing – review & editing, Validation. **Stéphane Debernard:** Writing – review & editing, Validation.

### Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

### Data availability

No data was used for the research described in the article.

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