Female receptivity in butterflies and moths
Centre for Ecology and Conservation, University of Exeter in Cornwall, Tremough Campus, Penryn TR10 9EZ, UK
e-mail: n.wedell{at}exeter.ac.uk
Accepted 4 July 2005
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Summary |
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Key words: receptivity, pheromones, sperm, ejaculate, sexual selection, PBAN, Acp, peptide
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Introduction |
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Male courtship |
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Anti-aphrodisiacs |
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One way in which males can reduce female receptivity is by rendering them
unattractive to rival males following mating. In some species, males release
pheromones that repel potential rivals (e.g.
Hirai et al., 1978;
Lecompte et al., 1998
). In the
butterfly Danaus gilippus, males release a pheromone-bearing dust
from their hair pencils containing a flight inhibitor (a ketone) and a `glue'
that stick the inhibitor onto the female's antennae
(Pliske and Eisner, 1969
;
Schneider, 1984
). This reduces
the likelihood that females mate again. Male butterflies and moths also
transfer chemical compounds, or anti-aphrodisiacs, to females at mating that
reduce their attractiveness. Male Heliconius erato butterflies
transfer a pheromone to the female, which she disseminates from special
storage organs called `stink clubs' making her highly distasteful to other
males (Gilbert, 1976
). These
odours are race-specific in this species, indicating they may be under
selection. In the green veined white Pieris napi butterfly, males
synthesize and transfer a volatile substance, methyl-salicylate, which is
emitted by mated females and acts as a strong deterrent to courting males
(Andersson et al., 2000
). This
reduces costly harassment by additional males, which is beneficial to females.
However, as males in this species transfer nutrients to females this gradually
turns into a conflict over remating, as females will eventually want to mate
again (Wiklund et al., 1993
).
In the related P. rapae, males also synthesize and transfer
anti-aphrodisiacs (methyl-salicylate and indole) to the female at mating
(Andersson et al., 2003
). Male
tobacco budworm also appears to transfer compounds that suppress female
attractiveness (Hendricks and Shaver,
1975
). These anti-aphrodisiacs only tend to have a transient
effect, as most females eventually remate.
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Mating plugs |
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Mechanical stimulation |
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Sperm |
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Male butterflies and moths produce two types of sperm: normal, fertilizing
`eupyrene' sperm, and a large number of non-fertile, anucleate `apyrene' sperm
(Meves, 1902;
Friedländer, 1997
).
Apyrene sperm are typically >90% of total sperm number
(Cook and Wedell, 1996
;
Solensky, 2003
), indicating
that they represent a substantial investment by males. Fertilizing sperm are
transferred in the spermatophore to the female in bundles containing 256 sperm
per bundle (Virkki, 1969
;
Phillips, 1970
;
Richard et al., 1975
;
Witalis and Godula, 1993
).
Apyrene sperm are highly active at ejaculation, whereas eupyrene sperm usually
remain in bundles. Apyrene sperm also appear to reach the female's spermatheca
before the fertile sperm in both butterflies and moths
(Silberglied et al., 1984
;
Tschudi-Rein and Benz, 1990
;
Watanabe et al., 2000
;
Marcotte et al., 2003
).
Non-fertile sperm seem to be critical to male reproductive success, because
males do not decrease investment in apyrene relative to eupyrene sperm when
reared on a restricted diet (Gage and
Cook, 1994
; Cook and Wedell,
1996
).
Various hypotheses have been proposed to explain apyrene sperm function
(reviewed in Silberglied et al.,
1984). Many of these suggest that apyrene sperm have a supporting
role, for example in aiding eupyrene sperm transport or activating the
eupyrene sperm (e.g. Osanai et al.,
1986
,
1987
;
Sahara and Takemura, 2003
).
Alternatively, they may represent a nutrient source either for the fertile
sperm in the spermatheca, or for the female and the developing zygotes.
However, Silberglied et al.
(1984
) have argued that these
hypotheses do not account for the fact that apyrene reach and persist within
the spermatheca and do not appear to be digested. If apyrene sperm were only
involved in eupyrene sperm transport or activation, it seems unlikely that
they would then be stored. If apyrene sperm have a solely supporting role, a
given number of non-fertile sperm should be needed for the activation or
transport of a single fertile sperm, and therefore the proportion of the two
sperm types should be constant within a species
(Cook and Gage, 1995
). This
does not appear to be the case. For example, in at least two species there is
a significant increase in the proportion of fertile sperm over the first two
matings: in Plodia interpunctella, the proportion of eupyrene sperm
increases from 7.5% to 10% (Gage and Cook,
1994
), and in Pieris rapae the increase is from 11% to
15% (Cook and Wedell,
1996
).
In their pioneering paper, Silberglied et al.
(1984) suggested that apyrene
sperm play a role in sperm competition, either by displacing or inactivating
rival males' sperm, or, by remaining in the females' spermatheca they may
delay female remating. Both these hypotheses predict that apyrene sperm
numbers should increase with increased risk of sperm competition. If apyrene
sperm displace or inactivate rival males' sperm, they may increase in response
to the presence of rival male sperm. In P. interpunctella, males
provide non-virgin females with more eupyrene, but not apyrene sperm
(Cook and Gage, 1995
), whereas
in the green-veined white butterfly Pieris rapae, males provide both
higher number of eupyrene and apyrene sperm to mated females
(Wedell and Cook, 1999
). On
the other hand, if apyrene sperm influences female sexual receptivity, we
expect their numbers to be related to female remating behaviour. It is of
course possible that non-fertile sperm may play both these roles.
A study on the polyandrous green-veined white butterfly P. napi,
suggests that the number of non-fertile sperm in the spermatheca is
responsible for inducing reduced female receptivity
(Cook and Wedell, 1999).
Females that do not remate store significantly more non-fertile sperm in their
spermatheca than remating females (Fig.
1). Moreover, the number of non-fertile, but not fertile, sperm
stored is positively related to the duration of non-receptivity. This suggests
that apyrene sperm are involved in influencing females' receptivity in the
P. napi by filling their sperm storage organ. There is genetic
variation in the tendency of females to store non-fertile sperm, which
correlates with the duration of their refractory period
(Wedell, 2001
). Similarly,
the reacquisition of female receptivity in the armyworm is associated with a
pronounced decline in the number of apyrene, but not eupyrene, sperm in
storage (He et al., 1995
), and
the presence of motile apyrene sperm in the spermatheca temporarily switches
off female receptivity in Heliothis zea
(Snow et al., 1972
). Females
may be able to detect the presence of sperm in their spermatheca (e.g. by the
presence of mechano-receptors; Lum and
Arbogast, 1980
), in order to ensure high fertility. Males may have
taken advantage of this system: rather than transferring many fertile sperm,
males transfer large number of apyrene sperm (that are highly motile and may
be cheaper to produce) that fill the females' sperm storage organ thereby
switching off receptivity. It is possible that production of apyrene sperm is
more efficient than a similar investment in fertile sperm to switch off female
receptivity, although this is yet to be confirmed.
|
In some species, larger females are more likely to mate multiply and hence
have elevated receptivity levels
(Torres-Vila et al., 1997;
Wedell and Cook, 1999
).
Bigger females have larger sperm storage organs
(Gage, 1998
), indicating they
may require receipt of more sperm to induce the same duration of
un-receptivity as smaller females. Intriguingly, male Plodia
interpunctella meal moths provide more sperm to bigger females
(Gage, 1998
). Increased
receptivity of larger females may also be due to having bigger reproductive
reserves that can be converted into more eggs and hence the need for
additional sperm. That is, larger females need more sperm and mate more
frequently.
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Seminal fluids |
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It is clear that substances transferred in the spermatophore play a role in
switching off female receptivity and stimulating oviposition and egg
maturation rate (Gillott,
2003). These substances often involve JH. In the moth
Heliothis virescens, female egg maturation is stimulated by JH
derived from males' accessory glands (Park
and Ramaswamy, 1998
). Similarly, in Cecropia silk moths,
males accumulate large amounts of JH that is stored in their accessory glands,
and later transferred to the female at mating (Shirk et al.,
1980
,
1983
). In addition, it appears
that male derived factors can stimulate the females' own production of JH
(Park et al., 1998
). Males
also transfer other substances apart from JH at mating that affect female
receptivity and reproductive physiology. In Helicoverpa zea and
H. armigera, factors from the male accessory gland stimulate egg
maturation and oviposition (Bali et al.,
1996
; Jin and Gong,
2001
).
In most moth species, receptive females attract males by releasing
pheromones during a characteristic `calling' phase. One important neuropeptide
controlling the production of sex pheromone in female moths is the female sex
Pheromone Biosynthesis Activating Neuropeptide (PBAN), which is mediated
either by humoral, hormonal or neural cues (e.g.
Raina, 1993;
Rafaeli, 2002
). Mating causes
cessation of female sex pheromone production in many moths: Helicoverpa
zea (Raina, 1989
),
Heliothis virescens (Ramaswamy et
al., 1996
), Lymantria dispar
(Giebultowicz et al., 1991
),
Argyrotaenia velutiana (Jurenka
et al., 1993
), Epiphyas postvittana
(Foster, 1993
), Bombyx
mori (Ando et al., 1996
),
Plodia interpunctella (Rafaeli
and Gileadi, 1999
), Choristoneura fumiferana and C.
rosaceana (Delisle and Simard,
2002
), by inhibiting PBAN production.
There is large variation between species in factors that affect female
pheromone production. In Helicoverpa zea, pheromone production is
switched off by a peptide originating from the male accessory glands
(Kingan et al., 1995), whilst
in the closely related species Heliothis virescens, a testicular
factor, most likely the ecdysteroid 20E, is responsible
(Ramaswamy and Cohen, 1992
;
Ramaswamy et al., 1996
). In
Choristoneura rosaceana, despite mating resulting in increased levels
of JH in females and suppressed pheromone production, this JH does not
originate from the male, as they lack the ability to synthesize and store JH
in their accessory glands (Cusson et al.,
1999
). In other moths, suppression of calling is triggered by a
neural signal, originating from the male, in the ventral nerve cord (e.g.
Bombyx mori, Ando et al.,
1996
; Lymantria dispar,
Giebultowicz et al.,
1991
).
In Helicoverpa zea, more than one factor controls the switch-off
of pheromone and the cessation of calling. Males transferring a spermatophore
without accessory gland products do not stop female pheromone production but
do stop the calling behaviour (Kingan et
al., 1993). In the silk moth, Bombyx mori, a combination
of both mechanical stimulation of the tip of the abdomen, which takes place
during copulation, together with successful receipt of sperm, trigger a neural
inactivation process that suppresses production of the female sex pheromone
bombykol (Karube and Kobayashi,
1999
). It seems that mechanical receptors at the tip of the
abdomen inhibit the release of PBAN
(Ichikawa, 1998
), whereas
there is no evidence that any further humoral factors transferred at mating
are involved. Similarly, in Lymantria dispar the insertion of male
genitalia during copulation causes a transient suppression of female pheromone
production, whereas sperm reaching the sperm storage organ are required for a
more permanent switch-off (Giebultowicz et
al., 1991
). Both the spermatheca and the bursa are innervated
(Raina et al., 1994
),
indicating the importance of an intact CNS for neural inactivation of
pheromone production. Cessation of calling in female moths appears in general
to be triggered by a combination of substances transferred in the ejaculate
(i.e. peptides, juvenile hormone) and neural elements (e.g. an intact ventral
nerve cord; Kingan et al.,
1995
; Ramaswamy et al.,
1996
; Marco et al.,
1996
; Delisle et al.,
2000
). In butterflies, potential seminal factors influencing
female receptivity remain largely unexplored.
Male-derived factors affecting female receptivity are common in insects. In
Drosophila melanogaster, for example, males transfer a cocktail of
>80 proteins and peptides (Acps) in the seminal fluid, which reduce female
receptivity and stimulate egg maturation and oviposition
(Wolfner, 2002;
Kubli, 2003
;
Chapman and Davies, 2004
). The
most intensively studied and characterised Acp is the sex peptide (Acp70A),
which reduces female receptivity and increases egg-laying by stimulating the
release of JH (Soller et al.,
1997
; Chapman and Davies,
2004
; Wigby and Chapman,
2005
). The effect appears to be caused by the C-terminal part of
the peptide. Intriguingly, D. melanogaster sex peptide
(DrmSP) has been found to increase JH production when injected in
female Helicoverpa armigera moths
(Fan et al., 2000
).
Furthermore, the C-terminal part of DrmSP reduces PBAN and pheromone
production in H. armigera females, whereas the N-terminal activates
CA production of JH (Fan et al.,
2000
).
The identification and characterisation of the male derived Pheromone
Suppression Protein in moths (HezPSP) has so far only been
demonstrated in Helicoverpa zea (Kingan et al.,
1993,
1995
;
Eliyahu et al., 2003
).
HezPSP shows no sequence homology to the Drosophila sex
peptide, apart from a disulphide bridge separated by an equal number, but
different amino acids (Eliyahu et al.,
2003
). Synthetic D. melanogaster SP (DrmSP)
stimulates JH production in the related H. armigera moths in
vitro in a similar way as in D. melanogaster
(Fan et al., 2000
), indicating
cross-reactivity of DrmSP in both suppression of pheromone production
and activation of JH production in H. armigera. Using
DrmSP-specific antiserum, immunoreactivity in male H.
armigera reproductive tissues was demonstrated. The antiserum was highly
N-terminal specific, indicating that this is the active region, whereas none
of the C-terminal peptides showed any immunoreaction
(Nagalakshmi et al., 2004
).
These results strongly indicate that endogenous H. armigera proteins
present in the male reproductive tract are responsible for stimulating
oviposition and suppressing female receptivity, resembling DrmSP.
In D. melanogaster the N terminus of DrmSP binds to sperm
(Kubli, 2003). Sperm function
both as a carrier and a reservoir of sex peptide by slowly releasing it while
stored in the female (Liu and Kubli,
2003
; Peng et al.,
2005
). Is it possible that non-fertile sperm in the Lepidoptera
may also be carriers of sex peptides in an analogous fashion to D.
melanogaster? The so-called `sperm effect' causing long-term suppression
of receptivity in D. melanogaster female requires successful transfer
and storage of sperm (Manning,
1972
). Similarly, in butterflies and moths sperm in storage (both
fertile and non-fertile) is required for inducing a long-term non-receptivity
(e.g. Giebultowicz et al.,
1991
; Karube and Kobayashi,
1999
; Cook and Wedell,
1999
).
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Conclusions and outlook |
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Another reason for variability across species in factors suppressing female
receptivity may be differences in their life histories. For example, JH is an
important regulator of migratory behaviours
(Rankin, 1991), which may
preclude its use by males as a means to stimulate female receptivity in
migratory species (e.g. Delisle et al.,
2000
), and hence favour employment of alternative molecules. There
is also growing evidence of substantial intra-specific genetic variation in
female remating behaviour. For example, in female Lobesia botrana
moths, multiple mating is a recessive, autosomally inherited trait
(Torres-Vila et al., 2002
).
There is also additive genetic variation in P. napi female remating
rate (Wedell, 2001
). In part,
genetic variation in mating rate may be a pleiotropic effect of variation in
metabolic rate, because genetically monogamous P. napi individuals
develop more slowly and lay eggs at a lower rate than genetically polyandrous
females (Wedell et al.,
2002
). The possibility that variation in female mating rate is
partly due to pleiotropy clearly needs further examination in this and other
taxa. In addition, genetic correlations of reproductive traits between the
sexes, either due to pleiotropy or sexually antagonistic alleles, are emerging
as an important force affecting the evolvability of reproductive traits such
as female receptivity (Rice,
2000
; Kirkpatrick and Hall,
2004
).
Intriguingly, there appears to be functional similarity between moth sex
peptides and the sex peptide of D. melanogaster. The exciting
possibility that seminal peptides have shared functionality in these two
disparate insect groups clearly needs further examination, and is an
intriguing research area waiting to happen. The question is: can we reconcile
the potentially conserved physiological pathways present across insect groups
with the observed rapid divergence of specific reproductive molecules within
species? This field is likely to see a rapid expansion in the near future,
given the development of new genomic and proteomic tools enabling detailed
examination of gene function, even in non-model taxa. Methods where specific
genes can be targeted, such as RNA interference knockdowns (e.g. Chapman et
al., 2003; Fabrick et al.,
2004; Wigby and Chapman,
2005
) and creation of null mutants using homologous recombination
(e.g. Liu et al., 2003), promise to be powerful techniques for exploring the
functional characterization of gene products involved in regulating female
receptivity in the Lepidoptera. The predicted research explosion will
hopefully shed some light on the extent to which seminal peptides are ancient
or rapidly evolving reproductive molecules in insects.
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Acknowledgments |
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