Arja Kaitala

Polyandry and its effect on female reproduction in the green-veined white butterfly (Pieris napi L.)

SummaryIn many insects nutrients transferred by the male to the female at mating are later incorporated into both the eggs and soma of the mated females. Accordingly, it has been suggested that female insects can use these male-derived nutrients both for somatic maintenance and to increase both the number and quality of their offspring. Moreover, much discussion is presently devoted to whether the male nuptial gift represents paternal investment, defined as “any increase in given males total surviving progeny by increasing the reproductive output by a given female”, or mating effort which obtains “if a male gains by increasing the proportion of eggs he fertilizes from a given female” (Parker and Simmons 1989). If the male nuptial gift represents parental investment it should be expected to benefit predominantly the offspring sired by the donor, whereas the “physiological fate” of the male nuptial gift is somewhat irrelevant under the mating effort explanation. In this paper we test these issues by studying the lifetime fecundity, egg weights and longevity of two groups of females of the polyandrous green-veined white butterfly, Pieris napi, one group of which was allowed to mate only once and the other of which was allowed to mate at liberty, the latter group of females mating on average 2.28 times. Moreover, to test the incorporation rate of male-derived nutrients, we performed a second set of experiments where females were allowed to mate with radioactively labelled males. The results showed that polyandrous females had higher lifetime fecundity compared to monandrous females, laying on average 1.61 as many eggs, and that the difference in cumulative fecundity between the two groups was statistically significant from the 5th day of egg-laying onwards. Polyandrous females also lived longer and maintained egg weight at a high level for longer than monandrous females. Largely concomitant with egg-laying rate, incorporation rate of male-derived nutrients peaked 3–4 days after mating, subsequently tapering off to stabilize at about 40% of the maximum. Given the opportunity, female P. napi remated after 3–5 days, the duration of the refractory period being positively correlated with ejaculate mass. Hence, although the nutrient investment of the first male to mate with a female “subsidizes” the progeny of later-mating males, the male nuptial gift in P. napi clearly qualifies as both paternal investment and mating effort.

Polyandrous female butterflies forage for matings

Butterfly mating systems exhibit great variation and range from strict monandry to strong polyandry. During mating males transfer ejaculates containing both sperm and accessory substances to females. In the polyandrous green-veined white butterfly, Pieris napi (Lepidoptera, Pieridae) these ejaculates average 15% of male body mass, but can represent up to 23% of body mass for individual males. Hence, mating is costly to males, and recently mated males increase copula duration but decrease ejaculate mass transferred to females. Substances transferred to females during mating are later incorporated into female soma and reproductive tissues, and multiply mated female butterflies have higher lifetime fecundity, lay proportionately larger eggs, and live longer compared to once mated females. Here we report that females of P. napi allowed to mate at liberty with recently mated males only (i.e. males that delivered a small ejaculate) increased their lifetime number of matings compared to females allowed to mate with virgin males only (i.e. males that delivered large ejaculates), the former group mating on average 5.1 times (range 2–10) and the latter group mating on average 2.8 times (range 1–4). The lifetime fecundity of the two groups of females did not differ significantly. Because nutrient donation from males is essential for females to realize their potential fecundity, we conclude that females of the polyandrous green-veined white actively forage for matings.

Female mate choice and mating costs in the polyandrous butterfly Pieris napi (Lepidoptera: Pieridae).

Males of the green-veined white butterfly (Pieris napi L.) transfer large ejaculates that represent on average 15% of their body mass when mating for a first time. Shortly after mating a male is able to transfer only a small ejaculate when mating a second time. Male ejaculate production plays a crucial role in the mating system ofP. napi because females use male-derived nutrients for egg production and somatic maintenance. Here we study how timing of female rematings and copulation duration are influenced by the mating history of their mates and, also, study if females exert mate choice to minimize their mating costs. Mating with a recently mated male increased female mating costs by increasing time in copula and mating frequency. Virgin females that mated with virgin males remated after an average of 6 days, whereas virgin females that mated with recently mated males remated after an average of 2 days. Moreover, copulations involving recently mated males lasted on average almost 7 h, whereas copulations involving virgin males lasted on average 2 h. Recently mated males were eager to remate, in spite of the fact that the size of the ejaculate they transfer is small and that they remain in copula for a long time. Hence it seems that males are more successful in the sexual conflict over mating decisions and that females do not minimize mating costs by choosing to mate preferentially with virgin males.

Natural variation in female mating frequency in a polyandrous butterfly: effects of size and age

Natural variation in female mating frequency in a polyandrous butterfly: effects of size and age.

Oviposition on the back of conspecifics : an unusual reproductive tactic in a coreid bug

Phyllomorpha laciniata (Heteroptera, Coreidae) is unique among terrestrial insects in that females lay eggs on the backs of conspecifics. Examination of >900 adult P. laciniata revealed that both males and females normally carry 1-15 eggs/individual, glued to their backs. On average, males carried twice as many eggs as females. Males captured while mating carried significantly more eggs than non-mating males, but mating females carried significantly fewer eggs than non-mating females. Eggs fare poorly in nature unless they are carried by a live conspecific. Marked adult bugs (n = 73) released live in the field retained 84% of the eggs when recaptured 5-7 d later, but all eggs attached on the backs of freshly killed males (n = 6) disappeared along with the bugs by the end of one day. Eighty-eight percent of eggs (n = 99) experimentally placed in Paronychia flowers disappeared within one day, and none remained after one week. Egg parasitism is a locally significant cause for egg mortality. Altogether 19% of old eggs (n=724) carried by individuals were parasitised by scelionid wasps (Gryon bolivari), and about one third of the individuals that carried old eggs had at least one parasitised egg. Females carried parasitised eggs relatively more often than males. The number of parasitised eggs increased with number of eggs carried but the probability of an individual egg being parasitised did not vary according to the number of eggs carried. Contrary to earlier reports, P. laciniata is not a species with exclusive paternal care because the eggs are commonly found on the backs of both sexes. The unequal occurrence of eggs between sexes and the association between number of eggs and an individuals mating status cannot be explained with the current knowledge. Laying eggs on the backs of other conspecific bugs is an effective way of decreasing egg mortality, although it is not perfect because of egg parasitism.

EGG LOAD AND MATING STATUS OF THE GOLDEN EGG BUG AFFECT PREDATION RISK

Females of the golden egg bug (Phyllomorpha laciniata) lay eggs on the backs of male and female conspecifics, and surprisingly, individuals commonly carry unrelated eggs. Here, we investigate predation risk from the ant Formica rufa during two reproductive stages of the golden egg bug: egg carrying and mating. Ants and an egg-loaded bug were enclosed with an unloaded bug, with a mating pair, or with a mating pair and an unloaded bug. Both mating and egg carrying increased predation risk. Mating increased predation risk because mating pairs were attacked more often than single egg-loaded bugs. When a mating pair was enclosed with an egg-loaded bug and an unloaded bug, the pair was attacked significantly more often than the two single individuals together, even though ant visitation rates did not differ among prey items. Ants attacked egg-loaded bugs significantly more often than unloaded bugs. Egg-loaded individuals suffered lower predation risks when in the presence of a mating pair than when in the presence of a single unloaded bug. Thus, predation risk depends on the mating status of nearby individuals. In the field, single individuals are often found with mating pairs; this observation could be explained if individuals decrease their predation risk by associating with preferred prey.

Is egg carrying attractive? Mate choice in the golden egg bug (Coreidae, Heteroptera)

In several species of fish, females select males that are already guarding eggs in their nests. It is a matter of debate as to whether a female selects a good nest site for her offspring (natural selection) or a male for his attractiveness (sexual selection). The golden egg bug, Phyllomorpha laciniata Vill, resembles fish in the sense that mating males carry more eggs than single males, but in the bugs, female mate choice is decoupled from egg site choice. The sexual selection hypothesis predicts that if females select males using male egg load as a cue for male quality, they should not mate with a male when eggs are removed, regardless of his mating attempts. When individual females were enclosed with an egg–loaded male and an unloaded male, they mated equally often with both males, although the loaded males courted more. In addition, when only successful males were used, females mated equally often with the loaded male and the unloaded male irrespective of sex ratio. Male choice rather than female choice affected mating frequency when sex ratio was equal. Therefore, females do not select the male by the eggs he carries, but successful males may receive many eggs due to egg dumping by alien females while they mate or as a consequence of mate guarding.

Joint brood guarding in parent bugs: an experiment on defence against predation

Females of Elasmucha grisea defend their eggs and small nymphs against invertebrate predators. Females sometimes guard their clutches side by side on the same birch leaf. We studied benefits of this joint guarding both in the field and in the laboratory. We found that adjacent females had significantly larger clutches than solitary females. In the laboratory, we studied the effectiveness of joint versus single defence against ant (Formica uralensis) predators. We established female pairs from initially singly guarding females by cutting off pieces of leaves with egg clutches and pasting them beside another female guarding her clutch. In the control group the females with their clutches were similarly cut off but these clutches were placed on another leaf without any female. The birch twigs where females guarded their clutches were placed in cages in close proximity to laboratory ant nests. In the experimental treatment, two females guarded their clutches together and at the same nest there was another birch twig without a female. In the control treatment two twigs with one female on each were placed close to another ant nest. Two females defended their clutches significantly more successfully, losing fewer eggs than did the single females. This primitive form of female sociality in parent bugs resembles colonial nesting in birds, where communal defence is also important. However, to our knowledge this is the first experiment where the benefit of joint guarding has been tested directly by manipulating the size of the breeding group rather than by measuring the risk of predation in groups of different size.

Counterstrategy to Egg Dumping in a Coreid Bug: Recipient Individuals Discard Eggs from Their Backs

The golden egg bug, Phyllomorpha laciniata Vill. (Heteroptera: Coreidae), is the only terrestrial insect in which females oviposit on the backs of female and male conspecifics. Eggs do not survive unless carried by a bug. Herein, I report laboratory observations that egg-carrying individuals actively brush their backs against the host plant seemingly in an effort to rub off eggs. Egg scraping is more common among individuals carrying many eggs than among those carrying only a few eggs. The most recently received eggs were rubbed off first. Females did not avoid laying eggs on the backs of egg-loaded individuals, nor did bugs carrying several eggs resist oviposition attempts more often than unloaded ones. Some males were likely to have fertilized the eggs they scraped off their backs. Laboratory results of active egg removal correspond with egg loss in the field, suggesting that egg scraping may explain egg loss in nature. The data indicate a cost of egg carrying to an individual and an evolutionary arms race between oviposition and discarding behavior.

Host-Plant Selection and Predation Risk for Offspring of the Parent Bug

Herbivores, especially specialists, must adapt to characteristics of their host to survive and reproduce successfully (Hardin and Tallamy1992). If offspring survival among different hosts varies, natural selection should lead females to choose egg-laying sites where performance of the progeny will be highest. This is especially true when newly hatched larvae cannot move to another host (Singer 1986), or when searching for new hosts would cause heavy mortality (Singer and Mandracchia 1982). A number of studies have shown that females that search for oviposition sites respond to plant characteristics that are correlated with the nutritional quality of plants for their offspring (e.g., Myers 1985, Damman and Feeny 1988). Also, secondary chemicals of plants play an essential part in determining whether the plant is suitable for oviposition (e.g., Feeny et al. 1985). Furthermore, females may detect visually or chemically the presence of other conspecific and nonconspecific competitors already on a potential host (Rothschild and Schoonhoven 1977, Rausher 1979, Mappes and Makela 1993). However, one of the most important selective agents driving the evolution of behavioral adaptations of prey animals is predation (Endler 1991), and for herbivorous insects, natural enemies commonly represent the major source of mortality (Myers 1981, Feeny et al. 1985). Thus, predation as well as plant characteristics could influence both oviposition behavior and offspring performance on the host (Bernays and Graham 1988). At the moment, however, there is very little empirical ev-