The roles of juvenile hormone and biogenic amines on
pheromone response plasticity and diapause
termination in male Caloptilia fraxinella
Joelle K. Lemmen* & Maya L. Evenden
Department of Biological Sciences, University of Alberta, CW405 Biological Sciences Building, Edmonton, AB,
Canada T6G 2E9
Accepted: 22 September 2015
Key words: methoprene, pyriproxyfen, reproductive diapause, electroantennogram, wind tunnel,
octopamine, dopamine, serotonin, Lepidoptera, Gracillariidae
Abstract In insects that exhibit a period of delayed reproduction, the timing of mating and reproduction is
controlled by environmental conditions that regulate endogenous factors such as hormones and bio-
genic amines (BAs). Caloptilia fraxinella (Ely) (Lepidoptera: Gracillariidae) undergoes a 9-month
reproductive diapause from adult eclosion in the summer until diapause termination the following
spring when adults mate. Male response to female sex pheromone is plastic, and is most acute when
moths are reproductively active. The aim of this study is to further elucidate the mechanisms
involved in the regulation of male response to pheromone in C. fraxinella, and to test whether the
application of BAs with and without a juvenile hormone analogue (JHA) to males in different physio-
logical states impacts pheromone responsiveness, as measured by electroantennogram and wind tun-
nel bioassays. Treatment of male C. fraxinella in reproductive diapause with one application of a
JHA induces the highest subsequent pheromone response in the fall, but does not alter pheromone
response earlier in reproductive diapause in the summer. The JHAs methoprene and pyriproxyfen
similarly enhance pheromone response in the fall. Treatment with methoprene alone or in combina-
tion with one of the BAs octopamine, dopamine or serotonin increases male pheromone responsive-
ness in the fall. The increase in pheromone response can be attributed to methoprene only, as
treatment with any of the BAs alone does not enhance male response to pheromone. Biogenic amine
treatment lowers male responsiveness to pheromone in some experiments, indicating that there may
be a role for BAs in maintaining low pheromone response during reproductive diapause in this
species.
Introduction
Long-lived insects can experience a reproductive inactivity
as adults during migration or diapause. In these species,
signalling systems for finding mates and oviposition loca-
tions should be plastic and most acute at reproductive
maturity and under suitable environmental conditions for
mating and offspring development (Anton et al., 2007). In
insects studied to date, induction of sexual communica-
tion with pheromones after reproductive inactivity is
under the regulation of exogenous factors such as temper-
ature and photoperiod that trigger endogenous regulating
factors including hormones (Goehring & Oberhauser,
2002; Anton et al., 2007).
Juvenile hormone (JH) is a sesquiterpenoid hormone
that regulates insect growth and development at all life
stages, and is well studied as an important gonadotropic
hormone in many Lepidoptera (Ramaswamy et al., 1997;
Minakuchi & Riddiford, 2006). Juvenile hormone regu-
lates male sex pheromone response and sex accessory
gland development in lepidopterans with delayed repro-
duction (Cusson et al., 1993; Duportets et al., 1996, 1998;
Ramaswamy et al., 1997; Denlinger, 2002; Anton et al.,
2007). The reproductive diapause of migratory monarch
butterflies, Danaus plexippus (L.), can be terminated with
JH application (Barker & Herman, 1976). Treatment with
a JH analogue (JHA) induces pheromone response of
newly eclosed male Agrotis ipsilon Hufnagel in a wind tun-
nel (Gadenne et al., 1993). Treatment with JHA affects the
sensitivity of central but not peripheral olfactory neurons
*Correspondence: E-mail: jlemmen@ualberta.ca
184 © 2016 The Netherlands Entomological Society Entomologia Experimentalis et Applicata 158: 184–201, 2016
DOI: 10.1111/eea.12391