Mating frequency and resource allocation to male and female function in the simultaneous hermaphrodite land snail Arianta arbustorum

Sex allocation theory predicts that mating frequency and long‐term sperm storage affect the relative allocation to male and female function in simultaneous hermaphrodites. We examined the effect of mating frequency on male and female reproductive output (number of sperm delivered and eggs deposited) and on the resources allocated to the male and female function (dry mass, nitrogen and carbon contents of spermatophores and eggs) in individuals of the simultaneous hermaphrodite land snail Arianta arbustorum. Similar numbers of sperm were delivered in successive copulations. Consequently, the total number of sperm transferred increased with increasing number of copulations. In contrast, the total number of eggs produced was not influenced by the number of copulations. Energy allocation to gamete production expressed as dry mass, nitrogen or carbon content was highly female‐biased (>95% in all estimates). With increasing number of copulations the relative nitrogen allocation to the male function increased from 1.7% (one copulation) to 4.7% (three copulations), but the overall reproductive allocation remained highly female‐biased. At the individual level, we did not find any trade‐off between male and female reproductive function. In contrast, there was a significant positive correlation between the resources allocated to the male and female function. Snails that delivered many sperm also produced a large number of eggs. This finding contradicts current theory of sex allocation in simultaneous hermaphrodites.     

Expandable spermatheca influences sperm storage in the simultaneously hermaphroditic snail Arianta arbustorum

Summary

In many simultaneously hermaphroditic land snail species, the sperm storage organ (spermatheca) is highly structured, suggesting that the female function might be able to influence offspring paternity. Physical properties of the sperm storage organ, including its initial size and sperm storage capacity, may also affect fertilization patterns in multiply mated snails. We examined the structure, volume and tubule length of empty spermathecae in the land snail, Arianta arbustorum, and assessed differences in spermatheca size following a single copulation. The number of spermathecal tubules ranged from 2–7, but was not correlated with the volume of empty spermathecae. The volume of sperm stored in the spermatheca after a copulation was correlated with neither the number of spermathecal tubules nor copulation duration. Mean spermathecal volume more than doubled between two and thirty-six hours after sperm uptake, but the length of the spermathecal tubules did not change. Interestingly, the volume of sperm stored in the spermatheca seems not to be related to the size of the spermatophore and thus not to the number of sperm received (= allosperm). The amount of allosperm digested in the bursa copulatrix was highly variable and no significant relationship with the size of the spermatophore received was found. These findings suggest that numerical aspects of sperm transfer are less important in influencing fertilization success of sperm in A. arbustorum than properties of the female reproductive tract of the sperm receiver.     

Effects of Intermating Interval on Spermatophore Size and Sperm Number in the Simultaneously Hermaphroditic Land Snail Arianta arbustorum

We examined the effect of intermating interval on spermatophore size and number of sperm delivered in the simultaneously hermaphroditic land snail, Arianta arbustorum . Snails that remated after 6–7 d transferred smaller spermatophores which contained fewer sperm than snails that remated after eight and more days. This indicates that individuals of A. arbustorum need at least 8 d to completely replenish their sperm reserves after a successful copulation. We suggest that the interval between two copulations is also influenced by the energy costs of the long-lasting courtship behaviour with extensive mucus production.     

The spermatheca in the land snail, Arianta arbustorum (Pulmonata: Stylommatophora): muscle system and potential role in sexual selection

Abstract. Previous studies have shown variable patterns of paternity after multiple mating, and also variation in sperm storage among individuals of Arianta arbustorum , which suggests that the spermatheca may influence paternity in this promiscuous land snail. To identify possible morphological correlates of sperm manipulation, we investigated arrangement and ultrastructure of the muscles of the spermatheca. The musculature surrounding the 2–9 spermathecal tubules is arranged in a complex three dimensional network. In addition, each tubule has a thin sheath in which longitudinally oriented cells make up the innermost layer. Usually, the smooth muscle cells are enclosed by connective tissue. Only occasionally is direct muscle-muscle contact established through dense plaques. The short thick filaments, their small diameter, the relatively weak development of the tubular system and sarcoplasmic reticulum, and the low density of mitochondria indicate that the muscle cells contract relatively fast but with little strength, that they recover slowly, and have low endurance. A single muscle cell may be innervated by several axons and one axon may contact several muscle cells. Combining evidence of the present paper and a foregoing investigation on the spermathecal epithelium, we suggest that the main function of the spermathecal muscles is to expel sperm stored for fertilization, while the ciliation of the common duct is probably responsible for the distribution of sperm among the tubules.     

Variation in multiple paternity and sperm utilization patterns in natural populations of a simultaneous hermaphrodite land snail

Mating frequency has important implications for patterns of sexual selection and sexual conflict, and hence for issues such as the maintenance of genetic diversity and speciation. We assessed the level of multiple paternity and sperm utilization patterns in four natural populations of the simultaneous hermaphrodite land snail Arianta arbustorum using four polymorphic microsatellite loci. A total of 1088 offspring from 26 wild‐caught snails were genotyped to determine the number of fathers siring each brood and paternity skew in succeeding clutches. Multiple paternity was detected in the offspring of all 26 mother snails examined with the contribution of two to six fathers. The four populations examined differed in the level of multiple paternity. Snails in the population with the highest density of adults showed the highest level of multiple paternity, whereas snails in the population with the lowest density exhibited the lowest value of multiple paternity. Highly skewed paternity patterns were found in the progeny of 15 (57.7%) of the 26 mother snails. The number and identity of fathers siring the offspring of single mothers also varied among successive clutches. Furthermore, genetic analyses indicate a low level of self‐fertilization in one of the four populations. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 350–361.     

Mating Frequency, Fecundity and Fertilization Success in the Hide Beetle, Dermestes Maculatus

While the immediate benefits accrued to females through multiple mating are well documented, the effect of sperm depletion for multiply mating males is rarely considered. We show that, in small mixed-sex laboratory aggregations, both male and female hide beetles, Dermestes maculatus (De Geer) mated multiply. There was considerable variation in the mating frequency of both sexes; however the skew in mating success was comparable for males and females. Several individuals that mated multiply also re-mated with a previous partner, but in a competitive environment no male copulated more than seven times. Mating success was unrelated to an individual's size, but males that had the most inter-sexual matings also engaged in the most intra-sexual mating attempts. In a second experiment, we show that, even in the absence of rivals, only a small number of males mated with all available virgin females. Moreover, even though males were mated twice to each female, males that copulated more than eight times failed to fertilize any eggs. We suggest that under natural conditions male hide beetles may refrain from mating either prior to, or at the point of, sperm depletion thereby reducing the selection pressure for females to discriminate against sperm depleted males. However, fecundity and fertilization success varied considerably across females and even those mating with sperm-replete males were unable to fertilize 100% of their egg batch. Thus, direct fertilization benefits accrued by females through mating more than once with the same male may play a key role in the maintenance of polyandry in this species.     

Population regulation in the land snail Arianta arbustorum: density effects on adult size,clutch size and incidence of egg cannibalism

Summary The relationships between local population density and adult size, clutch size and spatial distribution of egg batches were investigated in 11 natural populations of the land snail Arianta arbustorum in a forest near Uppsala, Sweden. Shell size of adults decreased with increasing population density as did clutch size. Within populations, clutch size scaled allometrically with shell size indicating size-specific fecundity. It is hypothesized that food unpalatability caused by mucus deposition slows down juvenile growth rate in high density populations, resulting in small adults and thus reducing their fecundity in subsequent years. The influence of the distance between batches on the incidence of egg cannibalism by hatchlings was examined in a laboratory experiment. In this experiment the number of eggs cannibalized increased with decreasing distance to the batch of hatching snails. Thus, in the field, eggs of highly aggregated batches suffer a high risk of cannibalism. In the 3 populations with the highest snail density, 21–39% of all batches were deposited close to each other (nearest neighbour distance 5 cm, i.e. less than hatchlings more within 1 day). These findings indicate that egg cannibalism can act as a population regulating factor.     

Effect of Mating Frequency on Female Fitness in Caloglyphus Berlesei (Astigmata: Acaridae)

We studied the effect of mating frequency on female longevity and fecundity in the mite Caloglyphus berlesei. We tested the hypothesis that high promiscuity is selected for in this species because females receive nutrients during copulation. Females were constantly exposed to either one or four males and fed either a standard or poor diet. The prediction that frequent mating benefits females was not confirmed. On the contrary, females kept with four males had significantly lower longevity on both diets and on the standard diet they also had decreased fecundity compared to females exposed to one male. On the poor diet the number of males had no significant effect on fecundity. Thus, increased mating frequency had a detrimental effect on female fitness.     

Mating strategy in Aleochara bilineata: sperm storage and allocation

Abstract By contrast to females that can maximize reproductive success with only one or a few copulations, males generally increase their fitness with frequency of mating. Sperm storage and allocation is therefore crucial for both male and female fitness. Sperm storage in Aleochara bilineata (Coleoptera; Staphylinidae) is investigated by measuring the number of spermatozoa stored in the female spermatheca after single, double or triple successive copulations with different males. The potential advantages of polyandry are studied in terms of the number of sperm stored by females mated twice with the same male (i.e. repeated copulation), compared with females mated twice with two different virgin males (i.e. polyandry). Level of polygyny is also estimated by measuring sperm allocation when ten successive mates are offered to a virgin male. Aleochara bilineata females store the sperm of the same or different males additively, suggesting no advantage for polyandry in terms of the number of sperm stored. A virgin male is able to inseminate ten different females but the number of sperm transferred decreases linearly. Finally, the latencies and durations of copulations are measured in all experiments to estimate changes according to the male or female status (i.e. virgin or mated). The latency before mating is higher when females are virgin than when females have already mated.     

Male Condition, Female Choice, and Extreme Variation in Repeated Mating in a Scaly Cricket, Ornebius aperta (Orthoptera: Gryllidae: Mogoplistinae)

Mating in the scaly cricket Ornebius aperta often includes the transfer of many spermatophores to individual females during extended copulatory interactions. We manipulated male condition in staged matings to determine whether this could explain variation in the number of repeated copulations seen across pairs. Males on a high nutrient diet were in good condition, were more likely to mate repeatedly, and transferred more spermatophores on average than low-diet males (in poor condition). High-diet males were more likely to produce a vibratory signal that increased female receptivity to repeated mating attempts. Courtship and copulatory interactions were always terminated by females, and in every case males had already formed a spermatophore when deserted by females. We conclude that variation in male repeated mating success may be due to female choice rather than an inability or unwillingness of low-diet males to produce spermatophores.     

Age-specific Effects of Novel Mutations in Drosophila Melanogaster II. Fecundity and Male Mating Ability

Evolutionary theories of senescence assume that mutations with age-specific effects exist, yet until now, there has been little experimental evidence to support this assumption. In this study, we allowed mutations to accumulate in an outbred, wild population of Drosophila melanogaster to test for age-specific differences in both male mating ability and fecundity. We assayed for age-specific effects of mutations after 10, 20, and 30 generations of mutation accumulation. For mating ability, we found the strongest effects of mutations in the first half of the life span after 20 generations, and at nearly all ages by generation 30. These results are qualitatively consistent with results from a companion study in which age-specific mortality was assayed on the same lines of D. melanogaster. By contrast, effects of fecundity were confined to late ages after 20 generations of mutation accumulation, but by generation 30, as with male mating ability, effects of novel mutations were distributed across all age classes. We discuss several possible explanations for the differences that we observe between generations within traits, and among traits, and the relevance for these patterns to models of aging as well as models of mate choice and sexual selection. This revised version was published online in July 2006 with corrections to the Cover Date.     

Clutch production in the darter Etheostoma lynceum and its implications for life-history study

We tested two hypotheses that describe previously untested assumptions about the appropriate stage(s) for use in determining clutch sizes in darters. Three sequential stages of clutch/ovarian development are recognized: mature oocyte/ovary, ripening oocytc/ovary, and ripe oocyte/ovary. Mean ratios of clutch size to female length (relative clutch size, RCS) were significantly smaller and variances of RCS were significantly greater in ripe females when compared to mature and ripening females. Correlation coefficients for the relationship between clutch size and standard length (S.L.) were significantly greater for mature and ripening females than for ripe females. Mean clutch size, adjusted for the S.L. covariate, was significantly greater in mature and ripening females than in ripe females. Thus, we conclude that counts of eggs from ripe females yield fecundity estimates that are lower and more variable than estimates from counts of oocytes from mature and ripening females collected at the same time. Based on this conclusion, we discuss methods for developing fecundity estimates in darters. Our results may be broadly applicable to other taxa of fishes with group-synchronous ovum development.     

Different effects of mating group size as male and as female on sex allocation in a simultaneous hermaphrodite

Sex allocation theory predicts that the optimal sexual resource allocation of simultaneous hermaphrodites is affected by mating group size (MGS). Although the original concept assumes that the MGS does not differ between male and female functions, the MGS in the male function (MGSm; i.e., the number of sperm recipients the focal individual can deliver its sperm to plus one) and that in the female function (MGSf; the number of sperm donors plus one) do not always coincide and may differently affect the optimal sex allocation. Moreover, reproductive costs can be split into “variable” (e.g., sperm and eggs) and “fixed” (e.g., genitalia) costs, but these have been seldom distinguished in empirical studies. We examined the effects of MGSm and MGSf on the fixed and variable reproductive investments in the sessilian barnacle Balanus rostratus. The results showed that MGSm had a positive effect on sex allocation, whereas MGSf had a nearly significant negative effect. Moreover, the “fixed” cost varied with body size and both aspects of MGS. We argue that the two aspects of MGS should be distinguished for organisms with unilateral mating.     

Repeated copulations as a strategy to maximize fertilization in the fly, Dryomyza anilis (Dryomyzidae)

In the fly, Dryomyza anilis, males copulate repeatedly withthe same female during oviposition. Each copulation bout consistsof intromission followed by several tapping sequences duringwhich the male touches the external genitalia of the femalewith his claspers. The relative fertilization success of thelast male to mate with the female increases with the numberof tapping sequences. In this study, male benefits of repeatedcopulation bouts were examined by comparing matings with thesame number of tapping sequences in one and several copulationbouts. The relative fertilization success for the last maleincreased with successive copulation bouts. Simulated ovipositionpatterns showed that fertilization success in matings with manycopulation bouts was higher than in matings with one bout onlyif eggs were distributed between bouts in a certain way. Thesepredicted oviposition patterns were compared with natural ones.Although males may benefit from repeated copulation, femalesare likely to prefer matings with quick oviposition. This intersexualconflict may also affect natural oviposition patterns. It issuggested that repeated copulation in D. anilis may have evolvedin connection with males trying to secure their paternity becausefemales can discharge sperm at any moment during mating.     

Male Mating History Influences Female Mate Choice in the Trinidadian Guppy (Poecilia reticulata)

Based on the phenotype‐linked fertility hypothesis, sexual selection should favour females that can accurately assess the recent mating history of available sexual partners and preferentially avoid mating with recently‐mated males [who may be sperm depleted (SD)] so as to minimize the risk of their eggs not being fertilized. This hypothesis has received to date only limited attention and empirical support. Therefore, in the current study, we investigated experimentally whether females of a vertebrate species, the Trinidadian guppy (Poecilia reticulata), are able to assess the recent mating history of males, and thus potentially their functional fertility, and choose to avoid mating with males that appear to have recently mated and who may be sperm limited. Individual virgin females were first given a dichotomous choice between a male that had not been recently observed to interact sexually with another female (i.e. not sperm‐depleted) and another male that had been observed to interact sexually with a female (i.e. potentially sperm‐depleted) as sexual partners. Paired males were matched for body length and coloration. Immediately following this test, the focal females were subjected to a free‐swimming mate‐choice test using the same paired stimulus males. As predicted, on average, female guppies avoided the apparently recently‐mated (and potentially sperm‐depleted) male and exhibited a significant preference for the other male not recently observed mating (and thus not likely sperm limited) during both tests. We do not yet fully understand the underlying mechanisms of this preference. Therefore, further research on the particular cues that females use to assess the recent mating history and fertility status of males is required.     

Dynamics of sperm storage in the grasshopper Eyprepocnemis plorans

Abstract. Sperm storage duration in the grasshopper Eyprepocnemis plorans Charpentier (Orthoptera, Acrididae) was found to be 58.5 days but with a wide between-female variation (from 26 to 113 days). One copulation was enough to fertilize two to eight egg-pods and to produce 130 eggs (28–313) and 119 embryos (28–290), on average. Sperm availability, however, decreased progressively with time, so that the majority of females spent a long final period of their lives without laying any pod. Finally, sperm storage duration was positively correlated with clutch size and total production of eggs and embryos.     

Male Remating Behavior and Its Effect on Female Reproductive Fitness in Cnephasia jactatana Walker (Lepidoptera: Tortricidae)

Male remating behavior and its effect on the female reproductive fitness of a New Zealand leafroller, Cnephasia jactatana, were investigated in the laboratory. With a recovery period of at least 24 h between matings, most males were able to mate four times and only about 25% could mate six times during their lifespan. Only 5% of males managed to mate twice within 1 day. Mated males transferred 31–51% smaller spermatophores than virgin males. When mating with a mated male, the female was subject to a 20–51% and 23–51% reduction in fecundity and fertility, respectively. With the increasing number of matings her partner had achieved before mating with her, the female's fertility declined significantly faster than fecundity. Courtship period and mating duration remained similar regardless of the male's mating history but males required increasingly longer latency to start courtship display with the increasing number of matings achieved.     

Trade-off between male and female allocation in the simultaneously hermaphroditic flatworm Macrostomum sp

Sex allocation theory for simultaneous hermaphrodites assumes a direct trade-off between the allocation of resources to the male and female reproductive functions. Empirical support for this basic assumption is scarce, possibly because studies rarely control for variation in individual reproductive resource budgets. Such variation, which can have environmental or genetic sources, can generate a positive relationship between male and female investment and can thus obscure the trade-off. In this study on the hermaphroditic flatworm Macrostomum sp. we tried to control for budget effects by restricting food availability in a standardized way and by using an inbred line. We then manipulated mating group size in a two-way design (two group sizes x two enclosure sizes) in order to induce phenotypic variation in male allocation, and expected to find an opposing correlated response in female allocation. The results suggest that we only managed to control the budget effects under some conditions. Under these the sex allocation trade-off emerged. Under the other conditions we found a strongly positive correlation between male and female allocation. We discuss possible causes for the observed differences.