Sex- and maturity-dependent antennal detection of host plant volatiles in the cabbage root fly, Delia radicum

Insect olfactory-guided behaviour is known to differ between males and females and to show strong plasticity as a function of adult maturity (age), and mating state (Gadenne et al., 2016). This plasticity helps insects to make optimal decisions when responding to sex pheromones, host-, food-, or oviposition site odours. In several moth species, recently mated male moths do not respond to female-emitted sex pheromones, because they would not be able to mate successfully (Gadenne et al., 2001). Blood-feeding insects such as mosquitoes and hematophagous bugs also adapt their responses to host odours as a function of age and mating state, thus avoiding taking unnecessary risks during the approach and attack of a host animal ((Gadenne et al., 2016) and references therein).

More recently, differences in behavioural responses to plant volatiles as a function of sex, maturity and mating state have been investigated in various phytophagous insects. In the fruit fly Bactrocera tyroni (Froggatt) (Diptera: Tephritidae), mated females were more attracted to their host fruit volatiles than unmated females (Devescovi et al., 2021). In the tomato fruit fly, Neoceratitis cyanescens (Bezzi) (Diptera: Tephritidae), both mated and unmated females responded to ripe tomato fruits, whereas males were rather attracted by odours from unripe fruits (Brevault and Quilici, 2010). In the cotton leafworm, Spodoptera littoralis (Boisduval) (Lepidoptera, Noctuidae), females moth change their behavioural preferences from flower odours to odours emitted by plants used for oviposition after mating (Saveer et al., 2012). As a last example, in several species, male moths are only rarely attracted by host plant volatiles, but host plant volatiles can synergize responses to the female-emitted sex pheromone (Masante-Roca et al., 2007, Ochieng et al., 2002, Reddy and Guerrero, 2004, Varela et al., 2011, Yang et al., 2004).

The physiological mechanisms underlying behavioural plasticity have been investigated in detail specifically in male moths responding to sex pheromones. Here, depending on the species, either changes in the peripheral or central olfactory system have been described ((Gadenne et al., 2016) and references therein). In the noctuid moth Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae), male responses to the sex pheromone increase with maturity, but not responses to plant volatiles (Greiner, 2002). However central, but not peripheral neuron responses to a flower volatile increased after mating in A. ipsilon, possibly facilitating a switch from searching for a mate to feeding behaviour (Barrozo et al., 2011). In some moth species, on the contrary, both peripheral and central nervous responses to host plant volatiles have been found to vary between sexes and as a function of maturity and mating state, in line with behavioural changes. For example in the grapevine moth Lobesia botrana (Denis and Schiffermüller) (Lepidoptera: Tortricidae), antennal lobe neurons in unmated males and in mated females responded more often to selected plant compounds than in mated males and unmated females (Masante-Roca et al., 2007). Antennal responses of Spodoptera littoralis females to plant odours, on the other hand, were generally stronger in unmated females as compared to mated females (Martel et al., 2009). Interestingly, glomerular responses to a flower odour measured by calcium imaging activity representing essentially receptor neuron responses in the same species decreased after mating, whereas glomerular responses to host plant volatiles (cotton) increased after mating (Saveer et al., 2012). Finally, differential expression of antennal olfactory genes has been shown in different insects, such as Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) and Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) after mating (Crava et al., 2019, Siciliano et al., 2014, Jin et al., 2017).

Adults of the cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae), feed from the nectar of a large diversity of plant species, whereas females are specialists of Brassicaceae plants for oviposition (Finch, 1989, Rännbäck, 2008). The cabbage root fly represents an interesting model to study sex differences and physiological plasticity in olfaction, because adults need several days to reach maturity and males and females might potentially respond differently to host-derived compounds, due to a differential role of host plants between the sexes. In addition to visual cues, females have been shown to use certain host plant-emitted odours, such as allyl isothiocyanate (AITC), to localize oviposition sites in the field (Tuttle et al., 1988). Also cis-3-hexenyl acetate, a volatile emitted by damaged host plants has been shown to be attractive for females (Kergunteuil et al., 2012). Other compounds such as dimethyl disulfide (DMDS) strongly decrease oviposition (Ferry et al., 2009, Kergunteuil et al., 2012, Lamy et al., 2017). Upon emergence and for the first few days of their life, unmated females and males search first for food sources and seem not to respond to host plant odours (Hawkes, 1975, Nottingham, 1988). Females usually start oviposition after a maturation phase that lasts about five days after emergence (Hawkes, 1975, Nottingham, 1988), but it is unknown whether this maturation, in addition to mating, contributes to changes in plant odour responses. Much less is known about how D. radicum males find their mating partners and if they use odour cues for orientation (Finch and Skinner, 1982). In particular, no sex pheromone has been identified so far. Males show some behavioural responses to AITC, but lower than females. This response could potentially help them to find a mating partner as this compound is only emitted by brassicaceous plants (Finch and Skinner, 1982) and mating usually takes place near the emergence site and therefore near the host plants (Coaker and Finch , 1971 in Nottingham, 1988). The main olfactory organ of D. radicum, the funiculus of the antenna, carries large numbers of four types of olfactory sensilla: trichoid, basiconic, grooved and clavate (Ross and Anderson, 1991, Ross and Anderson, 1987). Interestingly, female antennae carry about 40 % more sensilla than male antennae and lower sensillum numbers in males were observed for all types, which correlates with behavioural differences between sexes (Ross and Anderson, 1987).

As a basis for future behavioural and physiological studies, we examine here for the first time antennal responses of D. radicum to a selection of host-derived compounds using electroantennographic recordings. We reveal dose-dependent antennal responses for all tested compounds, showing that the tested compounds are all detected by the cabbage root fly antenna. Our secondary aim was to identify volatile organic compounds, previously identified from intact and damaged host plants, which might be detected differentially between the sexes or as a function of maturity, in order to choose compounds to investigate variation in behavioural responses in the future. To detect such potential differences, we compared dose-response curves and mean response amplitudes between sexes, and between recently hatched immature, and mature mated insects.

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