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Sourakov A., 2008. Pupal mating in Zebra longwing (Heliconius charithonia): photographic evidence. News of Lepidopterists’ Society. 50(1): 26-29, 32.
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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.
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text and photos ©Andrei Sourakov