Strategic sperm allocation in the Small White butterfly Pieris rapae (Lepidoptera: Pieridae) (original) (raw)
Related papers
Butterflies tailor their ejaculate in response to sperm competition risk and intensity
Proceedings of the Royal Society B: Biological Sciences, 1999
Males of many insects eclose with their entire lifetime sperm supply and have to allocate their ejaculates at mating prudently. In polyandrous species, ejaculates of rival males overlap, creating sperm competition. Recent models suggest that males should increase their ejaculate expenditure when experiencing a high risk of sperm competition. Ejaculate expenditure is also predicted to vary in relation to sperm competition intensity. During high intensity, where several ejaculates compete for fertilization of the female's eggs, ejaculate expenditure is expected to be reduced. This is because there are diminishing returns for providing more sperm. Additionally, sperm numbers will depend on males' ability to assess female mating status. We investigate ejaculate allocation in the polyandrous small white butter£y Pieris rapae (Lepidoptera). Males have previously been found to ejaculate more sperm on their second mating when experiencing increased risk of sperm competition. Here we show that males also adjust the number of sperm ejaculated in relation to direct sperm competition. Mated males provide more sperm to females previously mated with mated males (i.e. when competing with many sperm) than to females previously mated to virgin males (competing with few sperm). Virgin males, on the other hand, do not adjust their ejaculate in relation to female mating history, but provide heavier females with more sperm. Although virgin males induce longer non-receptive periods in females than mated males, heavier females remate sooner. Virgin males may be responding to the higher risk of sperm competition by providing more sperm to heavier females. It is clear from this study that males are sensitive to factors a¡ecting sperm competition risk, tailoring their ejaculates as predicted by recent theoretical models.
Male butterfly investment in successive ejaculates in relation to mating system
Behavioral Ecology and Sociobiology, 1996
In Lepidoptera, female mating systems range from strict monandry to strong polyandry. Males transfer an ejaculate during copulation that contains both sperm and accessory gland substances. In butterflies the male ejaculate has at least three effects: it (1) contains sperm that can fertilize the eggs of the male's mating partner, (2) influences the refractory period of the mated female, and (3) contains nutrients that can be used by the female to increase her reproductive output. A number of recent studies have shown that males in polyandrous mating systems are endowed with adaptations to increase mating capabilities. Relative to males in more monandrous species they transfer larger first ejaculates which contain relatively more protein, and allocate proportionally more resources to reproduction. The objective of this study was to compare male reproductive investment in successive ejaculates, in terms of both mass and quality, to determine if males of polyandrous species are capable of maintaining the production of larger and more nutritious ejaculates than males of more monandrous species. We used three species of pierid butterfly, with mating systems ranging from relative monandry to polyandry. The degree of polyandry had a substantial effect on the reproductive performance of males. The cumulative protein content of ejaculates increased with the degree of polyandry. Only males of the most polyandrous species, Pieris rapae, produced three successive ejaculates of similar mass and protein content. In the relatively monandrous species, Aporia crataegi and P. brassicae, males in subsequent matings never produced another ejaculate as large as that transferred by males mating for the first time, although the protein content (mg) of ejaculates did not differ in second and third ejaculates. Moreover, the ability to remate varied with the degree of polyandry. Given the opportunity to remate, the majority of P. rapae males mated three times, whereas relatively few A. crataegi and P. brassicae males were able to perform three matings. These results suggest that male capacity to produce large, nutritious ejaculates is limited in relatively monandrous species. In this study only males belonging to the most polyandrous species had the ability to recuperate quickly from a mating event and remate. Our results suggest that males in polyandrous systems are better adapted to mating more than once.
Behavioral Ecology and Sociobiology, 1986
Evidence suggests that males incur costs in producing ejaculates. Therefore some discrimination should be expected with respect to their pattern of allocating ejaculates. In a laboratory study, males of the European swallowtail butterfly Papilio machaon were mated with conspecific virgin females up to six times. The weight of the spermatophore and of the accessory substances delivered by males, the duration of mating, and the number of sperm in ejaculates were measured. The weight of the first spermatophore was related to male weight but that of accessory substances was not. The weight of the spermatophore delivered by males upon remating was always less than that of the first spermatophore. Second spermatophores produced by males were smallest when delivered on the day after the first mating and increased asymptotically to about half the initial size with time elapsed since the first mating. Copula duration was highest for males remating on the day after the first mating but decreased to the duration of the first mating for males that were remated on the third day after the first mating or later. The weight of accessory substances delivered by males and the number of sperm in ejaculates were also higher in first matings compared to all subsequent matings. Both of two males that were handpaired on three consecutive days after the first mating produced a cumulative ejaculate mass equalling that transferred at the first mating. Thus the fact that males delivered smaller ejaculates upon remating on the third day after the first mating or later requires explanation, especially in view of the fact that copulations were not prolonged. We argue that the male ejaculate delivery strategy in mildly polyandrous species should be to mate for the first time with virgin females, when a maximum size ejaculate should be delivered, and then to maximize the number of matings. The rationale behind the male shift towards smaller ejaculate sizes delivered at subsequent matings is that: (1) the size of the ejaculate that can be produced is dependent on the time elapsed since the last mating; (2) the abundance of virgin females decreases as the flight season proceeds; and (3) there is an inverse relationship between the size and number of ejaculates that a male can produce in his lifetime.
Insect Science, 2016
In butterflies, male reproductive success is highly related to the quality and the size of the spermatophore transferred to the female. The spermatophore is a capsule produced by the male during copulation, which in many species contains sperm in addition to a nuptial gift, and which is digested by the female after copulation. The nuptial gift may contribute to egg production and offspring quality, and in some cases also to female body maintenance. The production of the spermatophore, however, represents a cost for the male and, in polyandrous species, ejaculates are sometimes allocated adaptively across matings. Nonetheless, although the ecological factors affecting the reproductive success of female butterflies have been the topic of numerous studies, little information exists on the factors affecting males' contribution to reproduction, and the indirect impacts on female fecundity and fitness. We used the Glanville fritillary butterfly, Melitaea cinxia (Linnaeus, 1758) (Nymphalidae), in order to assess variation in male allocation to matings. In this species, smaller males produce smaller spermatophores, but variation in spermatophore size is not correlated with female reproductive success. We show that spermatophore size increases with male age at first mating, decreases with mating frequency and adult food-deprivation, and is not influenced by developmental food-limitation. The length of copulation period does not influence the spermatophore size nor influences the polyandrous mating behavior in this species. Male contribution to his spermatophore size is clearly influenced by his condition and adult-resource at the time of mating. Despite this variation, spermatophore size does not seem to have a direct impact on female reproductive output or mating behavior.
Protein content of spermatophores and male investment strategies in nectar-feeding butterflies
1996
The objective of this thesis was to investigate how male investment in ejaculates, both in terms of nutritional quality and sperm content, varies with the mating system in nectar-feeding butterflies. Protein content was determined using a dye-binding protein assay (Bio-Rad), and used as a measure of ejaculate quality. A comparative study on 11 species of butterflies from 2 genera was conducted to examine how male nutrient investment varied with female mating frequency (polyandry). Male ability to produce more than one large nutritious ejaculate was evaluated using three species of pierid that varied in the degree of polyandry. The cost of ejaculate production, in terms of recuperation time, was investigated in Pieris napi and Pieris rapae, two polyandrous species of pierid. Lastly, the effect of male body size on sperm precedence was examined using P. napi. I found that relative to males in monandrous systems, males in polyandrous systems transferred larger first ejaculates that con...
Males use sex pheromone assessment to tailor ejaculates to risk of sperm competition in a butterfly
Behavioral Ecology, 2009
In polyandrous butterflies males transfer a large, nutritious ejaculate at mating. Larger ejaculates delay female remating and confer an advantage in sperm competition. However, large ejaculates are costly, potentially selecting for male adjustment of ejaculate size to the risk of sperm competition. Here, we test if male ejaculate size in the butterfly Pieris napi varies with male density, and whether males assess sperm competition risk using the male sex pheromone citral as a cue. The results conformed to sperm competition theory and showed that male P. napi tailored their reproductive investment in response to the risk of sperm competition; ejaculates transferred by males in the high male density treatments were on average 23% larger than ejaculates transferred at low male densities. The results also show for the first time that the sex pheromone citral was used by males to assess male density; ejaculates transferred by males in presence of added male sex pheromone were 19% larger than ejaculates transferred in the control. In conclusion, the study shows how the sex pheromone not only facilitates female acceptance when dispensed by courting males but also allows males to assess the degree of male competition for matings.
Sperm precedence in monarch butterflies (Danaus plexippus)
Behavioral Ecology, 2009
We characterized sperm precedence in monarch butterflies (Danaus plexippus), using a series of experiments in which we manipulated male mating histories to vary spermatophore size and the number of sperm transferred. Several factors affected the outcome of sperm competition. There was a pattern of second-male sperm precedence, but second-male precedence was rarely complete, and several other factors had significant effects on paternity patterns. Larger males outcompeted smaller males when they were not matched for size. Phosphoglucose isomerase (PGI) genotype affected the outcome of sperm competition under very hot conditions. When sperm from the same pair of males competed in different females, males fared better when they transferred more sperm. These results demonstrate that sperm precedence within a species can be affected by many factors, including the circumstances under which it is measured.
Determinants of paternity in a butterfly
Proceedings of the Royal Society B: Biological Sciences, 1998
Success in sperm competition is of fundamental importance to males, yet little is known about what factors determine paternity. Theory predicts that males producing high sperm numbers have an advantage in sperm competition. Large spermatophore size (the sperm containing package) also correlates with paternity in some species, but the relative importance of spermatophore size and sperm numbers has remained unexplored. Males of the small white butter£y, Pieris rapae (Lepidoptera: Pieridae), produce large nutritious spermatophores on their ¢rst mating. On their second mating, spermatophores are only about half the size of the ¢rst, but with almost twice the sperm number. We manipulated male mating history to examine the e¡ect of spermatophore size and sperm numbers on male fertilization success. Overall, paternity shows either ¢rst male or, more frequently, second male sperm precedence. Previously mated males have signi¢cantly higher fertilization success in competition with males mating for the ¢rst time, strongly suggesting that high sperm number is advantageous in sperm competition. Male size also a¡ects paternity with relatively larger males having higher fertilization success. This may indicate that spermatophore size in£uences paternity, because in virgin males spermatophore size correlates with male size. The paternity of an individual male is also inversely correlated with the mass of his spermatophore remains dissected out of the female. This suggests that females may in£uence paternity by a¡ecting the rate of spermatophore drainage. Although the possibility of female postcopulatory choice remains to be explored, these results clearly show that males maximize their fertilization success by increasing the number of sperm in their second mating.
Behavioral Ecology and Sociobiology, 2006
Contrary to vertebrates, sperm production in insects may bear considerable costs for males. This is especially true in species that donate spermatophores containing sperm and nutrient-rich accessory gland products like in butterflies. Hence, spermatophores at first and subsequent copulations can differ in a quantitative and qualitative way. Such effects have particularly been shown in polyandrous species providing large spermatophores. Here we experimentally tested the effect of male mating status (virgin male vs recently mated male) on copulation duration, spermatophore size and females' fitness components in a monandrous butterfly Pararge aegeria that typically donates small spermatophores. Copulations with non-virgin males lasted on average five times longer than that with virgin males and resulted in a spermatophore which was on average three times smaller. Number of eggs laid and female life span were not affected by the mating status treatment, but there was a significant effect on the number of living caterpillars a female produced, as copulations with virgin males resulted in higher numbers of larval offspring. Interestingly, the difference in spermatophore mass at the first and the second copulation increased with male body size. This suggests differential spermatophore allocation decisions among males of different size. Consequences for females and potential mechanisms influencing female fitness components are discussed. Given the small absolute size of spermatophores in P. aegeria, components other than consumable nutrients (perhaps hormones) should cause the observed effects.