Click on the link to download and print pdf of the reference:
Sourakov A., 2008. Pupal mating in
Zebra longwing (Heliconius charithonia):
photographic evidence. News of
Lepidopterists’ Society. 50(1): 26-29, 32.
Pupal
mating in Zebra longwing, Heliconius charithonia
Pupal mating is a term that describes the behavior of butterfly males
seeking out female pupae prior to eclosion and
competing for the chance to mate with either phorate
(uneclosed) or with teneral
(freshly emerged) females. Pupal mating is known for many Heliconius species (Gilbert,
1991), but the behavior is otherwise unknown in the Lepidoptera, with the
single exception of a lycaenid, Jamenus evagoras (Elgar and Pierce, 1988). Also, in Heliconius,
the behavior arose only once in the course of evolution (all the pupal-mating species form a clade
together on the DNA-based evolutionary tree (Beltrán et al, 2007)).
Apparently, pupal mating is very well known from observations made in
insectaries, but it is observed infrequently in nature. The exception is Heliconius hewitsoni, which served as a
model in pupal mating study by Deinert et al. published in NATURE in 1991. The latter study suggested, for instance, that males with longer wings and shorter bodies should be
favored by selection. The attraction of males of Heliconius charithonia to female pupae was in great detail documented by a physician, Dr. Wm. Wittfeld, of south Florida in the late 19th century and published by his correspondent (Edwards, 1881). Here, I document that attraction and competition of males for female pupae as well as the process of actual pupal mating with the help of digital photography and filmography.
Observations made on Heliconius charithonia in northcentral Florida, Summer-Fall, 2007:
The attendance of female pupae by males begins at least a week prior to the
pupa becoming receptive. The persistence
of males has also been pointed out by Fleming et al. (2005), who state that
“males virtually ‘camped out’ in the garden waiting for female chrysalises to
become sexually receptive.” The latter
article, however, does not describe that ‘camping’ behavior in detail. In my observations, the males not only
visited and visually examined the same pupa for at least a week (Fig. C (see pdf)), but
also periodically swarmed it, with fighting occurring over the position on the
pupa (Fig. A and B (see pdf)). What would be
interesting to explore is whether pheromones have anything to do with the
cyclic nature of this behavior or whether the landing of one male on the pupa
triggers a similar competitive drive in other males. Turner (1981) attributes the ability to
locate pupae again and again to memory. Gilbert
(1976) provides circumstantial evidence that anti-aphrodisiacal pheromones
might be involved in repelling sexually active males from male pupae of H. erato
before eclosion, but does not discuss the role of
possible female pupal attractants. Males in my observations seemed to be well
aware of the pupal presence and whereabouts, but investigative
visits were initiated sporadically and so were ritual and actual fights over
position on the pupa. This fights
consisted of attempts by a male that first landed on pupa to fend off landing
of the next male by opening its wings. If such an attempt was unsuccessful, the attempts to throw the
competitor off using pressure of the head and antennae (Fig. B (see pdf)) were used. In the event that more males approached, the two
males on the pupae joined in their effort to fend them off by simultaneously
opening their wings (Fig. A (see pdf)), foregoing for the moment their own rivalry. Otherwise, they mostly maintained a closed
wing position as in Fig. D (see pdf). The
competitive behavior would end after one-two hours as abruptly as it would be
initiated, but would reoccur on the same pupa periodically throughout its
development.
In Fig. D and E (see pdf), the male on the left has successfully mated with the
female by inserting its abdomen into the pupa. Most of the time, there was just one more male positioned on the
pupa. That second male remained on the pupa
throughout the mating and participated in fending off other males by opening
its wings when the latter approached. Only for a brief moment in three hours of observations did I see the
second male inserting his abdomen into the pupa. The rest of the time, the abdomen of this
“companion” male was held bent backwards, though the claspers were sometimes
open and the abdomen was flexing sideways (Fig. F (see pdf)). Occasionally, one or two more males succeeded
in landing on the pupa, but due to insufficient grasp were dislodged shortly after
(Fig. G (see pdf)). I have little doubt that
similar observations have been made by the other researchers of Heliconius cited here; however, I found
no detailed description in the literature. It would be interesting to investigate the role of the “companion” male
in the population. Provided that mating
success was not coincidental but was achieved by a dominant male, the question
could be asked whether the “companion” male is the next in line in mate
competition, and whether within a population successful mating is achieved by a
small or large number of males.
Eventually, after two-three hours of mating, the female emerged (Fig. H,
I (see pdf)) while still in copula and remained
attached for at least another hour. The
female remained passive throughout the process, with the exception of spreading
of the wings and discharging meconium. The latter continued at a very slow rate
while in copula (Fig. J (see pdf)). Other males continued to approach the mating pair throughout (Fig. L (see pdf))
but with less and less frequency. They were always met with opening of wings by
the mated male, which were held open until the intruding males left. The mated pair remained sitting side by side
for some period of time even after copulation seized (Fig. K (see pdf)). At this point, no advances by other males
were observed. It was shown by Gilbert (1976)
on H. erato (which is also a pupal
mater) that males transfer anti-aphrodisiacs to females during copulation to
prevent future matings. Judging by my observations, this might be the
case in H. charithoniaas well.
View video footage of competition for female pupae by males of Heliconius charithonia.
References Cited
Beltrán M., Jiggins C. D.,
Bull V.,
Beltrán M., Jiggins C. D., A. V. Z. Brower, E. Bermingham, and J. Mallet. 2007. Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inference from multilocus DNA sequence data. Biological Journal of Linnean Society, 92: 221-239.
Deinert E. I. , Longino J. T., Gilbert L. E. 1994. Mate competition in butterflies. Nature 370: 23–24.
Edwards W. H., 1881. On certain habits of Heliconia charitonia, Linn., A species of butterfly found in Florida. Papilio, 1(11): 209-215.
Elgar M. A. and Pierce N. E. 1988. Mating
success and fecundity in an ant-tended lycaenid
butterfly. inReproductive Success: Studies of
individual variation in contrasting breeding systems (ed. Clutton-Brock T. H.)
Fleming T. H., Serrano D., Nassar J. 2005.Dynamics of subtropical population of the zebra longwing
butterfly Heliconius charithonia
(Nymphalidae).
Gilbert, L. E. 1975. Ecological
consequences of a coevolved
mutualism between butterflies and plants. In Coevolution of animals and plants, ed. L. E. Gilbert, P. H. Raven. Austin/London: Univ.
Gilbert L. E. 1976. Postmating female odor in Heliconius butterflies: a
male-contributed antiaphrodisiac? Science, 193: 419–420.
Gilbert L. E. 1991. Biodiversity of a Central American Heliconius community:
pattern, process, and problems. In: Price PW, Lewinsohn
TM, Fernandes TW, Benson WW, eds. Plant–animal
interactions: evolutionary ecology in tropical and temperate regions.
Penz CM. 1999. Higher level phylogeny for the passion-vine
butterflies (Nymphalidae, Heliconiinae) based on early stage and adult
morphology. Zoo. J. Linn. Soc. 127: 277-344.
Turner J. R. G. 1981. Adaptation and evolution in Heliconius: a defense of NeoDarwinism. Ann. Rev. Ecol. Syst., 12: 99-121.
text and photos ©Andrei Sourakov
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