Sperm Precedence Research Articles

THE ALLONEMOBIUS-WOLBACHIA HOST-ENDOSYMBIONT SYSTEM: EVIDENCE FOR RAPID SPECIATION AND AGAINST REPRODUCTIVE ISOLATION DRIVEN BY CYTOPLASMIC INCOMPATIBILITY

Evidence for the evolution of fertilization incompatibilities and rapid speciation can be biased by the occurrence of hybridization and reproductive endosymbionts such as Wolbachia. For example, patterns of mitochondrial DNA (mtDNA) variation can be obscured by mitotypes hitchhiking on extrachromosomal elements like Wolbachia, while such endosymbionts can also induce phenotypes that mirror the operation of intrinsic fertilization incompatibilities between species. Therefore, before strong inferences can be drawn concerning the rates and processes of speciation in arthropod systems, we must first assess whether extrinsic endosymbionts obscure patterns of speciation. Here, I use the Allonemobius fasciatus-socius species complex to determine what role Wolbachia has played in the presumed rapid divergence of this complex by analyzing patterns of mtDNA and nuclear DNA variation in conjunction with sequence and cytoplasmic incompatibility data on Wolbachia. Data on molecular variation suggest that Wolbachia has not induced a strong selective sweep of the mitochondrial genome; nor does Wolbachia appear to induce cytoplasmic incompatibility. Preliminary evidence indicates that a third species identified within this complex, A. sp. nov. Tex, is partially reproductively isolated from A. socius, its closest relative, via conspecific sperm precedence or some form of postzygotic isolation. Moreover, shared mitotypes between A. sp. nov. Tex and A. socius may indicate the occurrence of a hybrid zone between these species near the border of Texas and Louisiana, although they may also represent shared ancestral polymorphisms. Molecular data also indicate that all three species in this complex diverged from a common ancestor as recently as 3000–30,000 years ago. Finally, the radiation of this complex from its ancestral population likely occurred in the presence of one strain of Wolbachia, thus suggesting a minimal role for Wolbachia during this burst of speciation. In total, barriers to gene flow do appear to have evolved very rapidly in this group of crickets.

NO EVIDENCE THAT POLYANDRY BENEFITS FEMALES IN DROSOPHILA MELANOGASTER

Understanding the evolution of polyandry (mating with multiple males) is a major issue in the study of animal breeding systems. We examined the adaptive significance of polyandry in Drosophila melanogaster, a species with well-documented costs of mating in which males generally cannot force copulations. We found no direct fitness advantages of polyandry. Females that mated with multiple males had no greater mean fitness and no different variance in fitness than females that mated repeatedly with the same male. Subcomponents of reproductive success, including fecundity, egg hatch rate, larval viability, and larval development time, also did not differ between polyandrous and monogamous females. Polyandry had no affect on progeny sex ratios, suggesting that polyandry does not function against costly sex-ratio distorters. We also found no evidence that polyandry functions to favor the paternity of males successful in precopulatory sexual selection. Experimentally controlled opportunities for precopulatory sexual selection had no effect on postcopulatory sperm precedence. Although these results were generally negative, they are supported with substantial statistical power and they help narrow the list of evolutionary explanations for polyandry in an important model species.

Sperm competition in Odonata (Insecta): the evolution of female sperm storage and rivals' sperm displacement

AbstractOdonates (dragonflies) are well known for the ability of the males to displace sperm stored in the female's sperm‐storage organs during copulation. By this means, copulating males are able to increase their fertilization success. This ability has been used as an example to illustrate a conflict of interests between the sexes in which males have evolved sperm‐displacement mechanisms whilst females have presumably evolved means to avoid sperm displacement. The present review has four aims: (1) to describe the copulatory mechanisms used during sperm displacement; (2) to analyse the causes of sperm usage patterns; (3) to discuss this information using current hypotheses on conflict between the sexes; and (4) to illuminate topics for further research. Four copulatory mechanisms are described: sperm removal (physical withdrawal of stored sperm), sperm repositioning (‘pushing’ of rival sperm to sites where its use will be least likely), female sensory stimulation to induce sperm ejection, and sperm flushing (displacement of sperm using the copulating male's sperm). Sperm‐precedence studies in Odonata are scarce and their values vary considerably between species. In those species in which sperm displacement is incomplete, the last copulating male obtains a high but variable short‐term fertilization success which decreases with time. Some male and female factors affecting sperm precedence patterns are mentioned: (1) male variation in genital morphology; (2) duration of copulation influenced by the male (the longer the copulation, the more stored sperm displaced); (3) adaptations of the sperm‐storage organs that allow the female to manipulate the sperm she has received (i.e. avoiding sperm displacement, re‐distributing sperm masses, favouring sperm located in certain sites and ejecting sperm after copulation). We suggest that male and female odonates have co‐evolved at the level of genital function with the control of stored sperm as the focus of the conflict. The benefits for males in this co‐evolution lie in maximizing their fertilization success. However, it is not clear what females obtain from storing sperm and making it unreachable during sperm displacement. Two hypothetical benefits that females may obtain for which some evidence has been gathered are genetic diversity and viability genes. It is finally suggested that odonates can become excellent subjects of study for testing current ideas related to sexual conflict and speciation processes through sexual selection.

Sperm Precedence in Colorado Potato Beetle, <I>Leptinotarsa decemlineata</I> (Coleoptera: Chrysomelidae): Temporal Variation Assessed by Neutral Markers

Variation in sperm precedence was examined in the Colorado potato beetle, Leptinotarsa decemlineata Say, using neutral allozyme markers. Two temporal components were studied: (1) pairing duration and (2) time since initial pairing. We used two pairing protocols that differed in the time males and females were allowed to mate for first and second pairings. When pairings were limited to 8 h each for the first and second male, the proportion of offspring in the xth egg mass attributable to the second male, P2(x), rose from 68% in the first egg mass after pairing with the second male to 78% in the tenth egg mass. When pairing was extended so that the first male-female pair had time to produce three egg masses and the second male was allowed to remain with the female indefinitely, P2(x) rose from 44% in the first egg mass after pairing with the second male to nearly 100% in the third and subsequent egg masses. Observations that (1) multiple matings are necessary to fill the female’s spermatheca and (2) the last male accounts for a greater proportion of offspring with time, provide evidence for both the sperm mixing and sperm displacement hypotheses. These data also help to explain male-guarding behavior in Colorado potato beetle. Because the allozyme markers were shown to be neutral with respect to fitness, other aspects of mating behavior could be tested by establishing a similar series of unique lines.

Pollination of Anthurium (Araceae) by derelomine flower weevils (Coleoptera: Curculionidae)

Cyclanthura flower weevils (Coleoptera: Curculionidae: Derelomini) are identified for the first time as pollinators of multiple species of Anthurium (Araceae) in Costa Rica. The weevils are present on the inflorescences in small numbers during the pistillate and staminate phase of anthesis, and consume plant tissues and pollen. The individuals of one species of Cyclanthura can visit several Anthurium species within the same locality. They also engage in reproductive activities and are likely to oviposit into the flowers. The mating strategies suggest that sperm precedence selects males that are able to secure their position as the last partner prior to oviposition.

Sexual selection in a simultaneous hermaphrodite with hypodermic insemination: body size, allocation to sexual roles and paternity

Theory predicts that variation in body size within a population of simultaneous hermaphrodites should affect sex allocation, leading to individual differences in mating strategies and increased investment in female function with size. Small animals with fewer resources should invest proportionally more of their resources in male function than large animals, resulting in sperm displacement and paternity patterns that are independent of body size. This study investigated the effect of body size on mating patterns, egg production (an indirect measure of sperm transfer) and paternity in Alderia modesta, a sperm-storing, hermaphroditic sea slug with hypodermic insemination. The relative sizes of two hermaphrodites affected the probability and duration of inseminations; smaller animals inseminated larger mates for longer than vice versa. Sperm transfer began at a smaller size and age than egg production, and estimates of both sperm transfer and egg production increased with body size. Paternity patterns varied widely; in this species, unpredictable sperm precedence patterns may be a consequence of hypodermic insemination and the lack of a well-defined sperm storage organ. Hypodermic injections across all sections of the body successfully transferred sperm and fertilized eggs. The function and consequences of hypodermic insemination are discussed. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

Number of mating males and mating interval affect last-male sperm precedence in Tenebrio molitor L.

Polyandrous females often mate with more than two males, and yet most studies of postcopulatory sexual selection involve only two males. In insects, second-male sperm precedence is usually taken as evidence of overall last-male sperm precedence despite some studies to the contrary. Furthermore, the processes or mechanisms causing the patterns are often unknown and yet are important when estimating how postcopulatory sexual selection might act on males. Whether the patterns and processes change in normal sperm competitive situations and the effects of other factors besides mating order need to be examined to better assess the evolutionary potential of postcopulatory sexual selection. In this study, I assessed the effects of mating interval and number of mating males on sperm precedence patterns and their causal mechanisms in the mealworm beetle, Tenebrio molitor. Last-male sperm precedence was the same when two or three males mated, but also depended on mating intervals and hence mechanisms of paternity bias. However, when females mated with many males, one of the mechanisms no longer created last-male sperm precedence. This example illustrates the importance of knowing both the patterns and mechanisms of paternity bias and whether they change depending on female mating frequency to make reasonable inferences about the potential for postcopulatory sexual selection on males. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

Multiple mating, paternity, and body size in a simultaneous hermaphrodite, Aplysia californica

Sperm displacement and sperm competition prove difficult to measure, but are crucial elements in predicting sex allocation strategies of sperm-storing hermaphrodites. Body size is predicted to affect sex allocation so that within a population, large animals invest a greater proportion of resources in female function than do small animals. These mating strategies depend on sperm displacement abilities and lead to similar levels of paternity across body sizes despite differences in resource level. The present study investigated mating patterns, multiple paternity, and sperm competition in a field population of a simultaneously hermaphroditic sea slug, Aplysia californica (California sea hare). Animals mating in the female role were larger than the mean for the population, indirectly supporting theoretical predictions for increased investment in female function with body size. However, contrary to predictions, animals mating in the male role were not different in size from the population mean or the animals they inseminated. Individual tagging revealed that sea slugs are capable of moving across distances that allow for the sampling of many potential mates, and that they mate repeatedly in both sexual roles. Microsatellite paternity analysis demonstrated that multiple mating in the field leads to multiple paternity, and last-sperm donors achieve high levels of paternity. There was no effect of body size on paternity. Further paternity studies are needed to reveal the mechanisms of sperm precedence patterns in A. californica. Copyright 2003.

Male Competition over Access to Females in a Spider with Last‐Male Sperm Precedence

AbstractAgonistic behaviour between male cellar spiders (Pholcus phalangioides) was investigated to test whether (1) size difference determines which male achieves access to the female, (2) males are able to monopolize access to the female until egg laying and whether (3) female resource value increases before egg laying because of last‐male sperm precedence. We further investigated whether (4) there is variation in time and energy spent on courtship and copulation depending on the degree of sperm competition, i.e. with or without rival present. In three experimental settings we introduced two males of either different or similar sizes, or a single male to a female. The mating units were constantly video‐observed until the females produced their first egg sac. Experience, ownership and female resource value in terms of body size was controlled. Our results show that larger males achieve almost exclusive access to females. Size symmetrical settings resulted in increased fighting activity and duration but dominance did not influence mating success. If copulations were disturbed by the rival male, copulations were terminated earlier in symmetrical settings compared with asymmetrical settings. In 94.8% of trials only one copulation took place, suggesting that the copulating male successfully monopolized access to the female. Males confronted with a rival copulated longer but courted significantly shorter than lone males. Although the last male to copulate sires 88% of the offspring in P. phalangioides, neither fighting nor courtship activity increased before the female laid a batch of eggs. This suggests that males have no indication of the timing of oviposition.

The evolution of conspecific sperm precedence in Drosophila.

Conspecific sperm precedence takes place when females inseminated by both conspecific and heterospecific sperm preferentially produce conspecific rather than hybrid offspring. Although many studies have documented conspecific sperm precedence, most have only identified it between taxa that are already considered to be good species. Here, we test for sperm precedence between two Drosophila pseudoobscura subspecies and between two Drosophila melanogaster races to evaluate how early in evolutionary divergence sperm precedence evolves. We found evidence of weak conspecific sperm precedence between the Drosophila subspecies but none between the Drosophila races. These pairs of taxa are already separated by mating discrimination and/or hybrid sterility, so our observation suggests that conspecific sperm precedence does not always evolve before other barriers to gene exchange.

Experimental Evidence for the Evolution of Numerous, Tiny Sperm via Sperm Competition

Sperm competition, when sperm from different males compete to fertilize a female's ova [1], is a widespread and fundamental force in the evolution of animal reproduction [2]. The earliest prediction of sperm competition theory was that sperm competition selected for the evolution of numerous, tiny sperm, and that this force maintained anisogamy [3]. Here, we empirically test this prediction directly by using selective breeding to generate controlled and independent variance in sperm size and number traits in the cricket Gryllus bimaculatus. We find that sperm size and number are male specific and vary independently and significantly. We can therefore noninvasively screen individuals and then run sperm competition experiments between males that differ specifically in sperm size and number traits. Paternity success across 77 two-male sperm competitions (each running over 30-day oviposition periods) shows that males producing both relatively small sperm and relatively numerous sperm win competitions for fertilization. Decreased sperm size and increased sperm number both independently predicted sperm precedence. Our findings provide direct experimental support for the theory that sperm competition selects for maximal numbers of miniaturized sperm [3]. However, our study does not explain why G. bimaculatus sperm length persists naturally at ∼1 mm; we discuss possibilities for this sperm size maintenance.

Experimental analysis of the mating system of the white pine weevil,Pissodes strobi(Peck) (Coleoptera: Curculionidae)

The white pine weevil, Pissodes strobi, severely restricts the growth and range of Sitka spruce (Picea sitchensis) in British Columbia. Knowledge of the patterns of male and female mating success is important for designing biocontrol programs and for understanding the reproductive potential of this weevil. To examine patterns of male and female reproductive success, we performed experiments in which the numbers of competing mates were varied, and used microsatellite markers to assay for mating success. Matings were conducted under four regimes: two males competing for a female, four males competing for a female, two females competing for a male, and four females competing for a male. We assayed 1869 progeny among several replicates for four marker loci. We found considerable multiple paternity, and the variance of reproductive success was higher in males than in females. The normalized variance of male success was higher among four competing males than between two competing males, which is consistent with last-male sperm precedence, while the normalized variance of female success was independent of female number for a constant male number, indicating that sperm quantity was not a limiting factor for reproduction at these mate densities.

Female age and sperm competition: last-male precedence declines as female age increases

Until very recently, most studies of sperm competition have focused on variation in male competitive ability. However, we now know that a number of reproductive traits, including oviposition rate, use of stored sperm and receptivity to mating, vary with female condition. Because females can play an active part in the movement of sperm within their reproductive tract, sperm competition may be influenced by female condition. Existing studies of sperm competition in fruitflies ignore the effects of female condition, using females that are 3-4 days old and in their reproductive prime. But condition will decline as a female senesces. Here, we examine the effect of female age on the outcome of sperm competition in three strains of the fruitfly, Drosophila melanogaster. Previous studies have shown that female age influences preference for mates and male ejaculation strategies. In this study, we find that when males are mated to females that are older than 17 days, last-male sperm precedence decreases significantly. These results could lead to a greater understanding of the physiological mechanisms that regulate the outcome of sperm competition.

Prolonged mate guarding and sperm competition in the weevil Diaprepes abbreviatus (L.)

The hypothesis that prolonged copulatory mate guarding coexists with last male sperm precedence was tested for the sugarcane rootstalk borer weevil, Diaprepes abbreviatus (L.) (Coleoptera: Curculionidae). Male D. abbreviatus showed a long copulatory guarding. Both males and females were less likely to remate when prolonged guarding occurred compared with terminating copulation early. Guarding was generally terminated by the struggling behavior of the female. Mating experiments using normal and sterile (X-ray irradiated) males revealed a similar value of last-male sperm precedence for both irradiated and normal males. The P-sub-2 values of normal and sterile males were similar when all oviposited eggs were counted over 30 days. These data made it possible to calculate the expected gain to a male from prolonged guarding compared with leaving a female early and seeking out an additional mate. We show that guarding has the higher fitness. Eggs were deposited in clutches in which normal fertilized eggs were grouped together and were attached to a group of sterile eggs. This, together with identifying the form of the cul-de-sac typespermatheca, allowed us to suggest a unique repositioning process, which has not been described elsewhere, as the likely mechanism by which last-male sperm precedence was achieved. Copyright 2003.

Phenology and biology of harvestmen in and near Sapporo, Hokkaido, Japan, with some taxonomical notes on Nelima suzukii n. sp. and allies (Arachnida: Opiliones)

Phenology and biology of a total of 11 opilionid species were surveyed in and near Sapporo, Hokkaido. Most of the species showed an annual life cycle with overwintering in egg stage. Exceptions were Paraumbogrella pumilio having an annual cycle with adult hibernation and Sabacon makinoi with overwintering in both egg and juvenile stages. Compared to the phenological patterns of opilionid assemblage in Shikoku, southwestern Japan, those in Hokkaido were characterized by the absence of species with overwintering in juvenile stage. Among the species overwintering as eggs, species whose juveniles emerge earlier in spring tended to have longer juvenile period. Furthermore, in most of the species females reached adulthood earlier than males (protogyny). The protogyny seems to be rather prevalent in harvestmen of the superfamily Phalangioidea including Phalangiidae and Sclerosomatidae, although it has been only rarely documented in insects and other arachnids. Long reproductive period and multiple mating by females connected with presumable last sperm precedence might explain protogeny in harvestmen. Except for three soil-dwelling species (Sabacon makinoi, S. imamurai, and Paraumbogrella pumilio), all species changed their diurnal microhabitat preference from soil litter on the ground to upward herbaceous layer or tree trunks before they reach adulthood. Even in sexually reproducing species, adult sex ratios in the field often deviated from 1:1. Relative abundance between male and female changed also temporally, probably as a result of sexual difference in microhabitat preference and in reproductive behavior. Data on fecundity of some species and egg size of ten species were presented. Mucous egg sacs produced by two Sabacon species are described and illustrated for the first time. In addition, a new name Nelima suzukii is proposed for one of the two species of the genus Nelima, with some notes on their taxonomy and biology.

Reproductive behaviour of Odonata: the history of a mystery

Abstract The main, externally visible components of odonate reproductive behaviour were known from published accounts for about 300 years before sperm displacement during copulation was first described. The latter discovery, revealed by Jonathan Waage in 1979, revolutionised the interpretation of odonate reproductive behaviour, allowing it for the first time to be interpreted convincingly in the context of sexual selection and the evolution of mating systems. This insight has been a prerequisite for elegant, ongoing work on mechanisms of sperm displacement and sperm precedence in Odonata.

Linear models for assessing mechanisms of sperm competition: the trouble with transformations.

Although sperm competition is a pervasive selective force shaping the reproductive tactics of males, the mechanisms underlying different patterns of sperm precedence remain obscure. Parker et al. (1990) developed a series of linear models designed to identify two of the more basic mechanisms: sperm lotteries and sperm displacement; the models can be tested experimentally by manipulating the relative numbers of sperm transferred by rival males and determining the paternity of offspring. Here we show that tests of the model derived for sperm lotteries can result in misleading inferences about the underlying mechanism of sperm precedence because the required inverse transformations may lead to a violation of fundamental assumptions of linear regression. We show that this problem can be remedied by reformulating the model using the actual numbers of offspring sired by each male, and log-transforming both sides of the resultant equation. Reassessment of data from a previous study (Sakaluk and Eggert 1996) using the corrected version of the model revealed that we should not have excluded a simple sperm lottery as a possible mechanism of sperm competition in decorated crickets, Gryllodes sigillatus.

SPERM COMPETITION MECHANISMS, CONFIDENCE OF PATERNITY, AND THE EVOLUTION OF PATERNAL CARE IN THE GOLDEN EGG BUG (PHYLLOMORPHA LACINIATA)

Theoretical models predict how paternal effort should vary depending on confidence of paternity and on the trade-offs between present and future reproduction. In this study we examine patterns of sperm precedence in Phyllomorpha laciniata and how confidence of paternity influences the willingness of males to carry eggs. Female golden egg bugs show a flexible pattern of oviposition behavior, which results in some eggs being carried by adults (mainly males) and some being laid on plants, where mortality rates are very high. Adults are more vulnerable to predators when carrying eggs; thus, it has been suggested that males should only accept eggs if there are chances that at least some of the eggs will be their true genetic offspring. We determined the confidence of paternity for naturally occurring individuals and its variation with the time. Paternity of eggs fertilized by the last males to mate with females previously mated in the field has been determined using amplified fragment length polymorphisms (AFLPs). The exclusion probability was 98%, showing that AFLP markers are suitable for paternity assignment. Sperm mixing seems the most likely mechanism of sperm competition, because the last male to copulate with field females sires an average of 43% of the eggs laid during the next five days. More importantly, the proportion of eggs sired does not change significantly during that period. We argue that intermediate levels of paternity can select for paternal care in this system because: (1) benefits of care in terms of offspring survival are very high; (2) males have nothing to gain from decreasing their parental effort in a given reproductive event because sperm mixing makes it difficult for males to reach high paternity levels and males are left with no cues to assess paternity; (3) males cannot chose to care for their offspring exclusively because they can neither discriminate their own eggs, nor can they predict when their own eggs will be produced; and (4) males suffer no loss of further matings with other females when they carry eggs. Thus, our findings do not support the traditional view that paternal investment is expected to arise only in species where confidence of paternity is high. The results suggest that females maximize the chances that several males will accept eggs at different times by promoting a mechanism of sperm mixing that ensures that all males that have copulated with a female have some chance of fathering offspring, that this probability remains constant with time, and that males have no cues as to when their own offspring will be produced.

LINEAR MODELS FOR ASSESSING MECHANISMS OF SPERM COMPETITION: THE TROUBLE WITH TRANSFORMATIONS

Although sperm competition is a pervasive selective force shaping the reproductive tactics of males, the mechanisms underlying different patterns of sperm precedence remain obscure. Parker et al. (1990) developed a series of linear models designed to identify two of the more basic mechanisms: sperm lotteries and sperm displacement; the models can be tested experimentally by manipulating the relative numbers of sperm transferred by rival males and determining the paternity of offspring. Here we show that tests of the model derived for sperm lotteries can result in misleading inferences about the underlying mechanism of sperm precedence because the required inverse transformations may lead to a violation of fundamental assumptions of linear regression. We show that this problem can be remedied by reformulating the model using the actual numbers of offspring sired by each male, and log-transforming both sides of the resultant equation. Reassessment of data from a previous study (Sakaluk and Eggert 1996) using the corrected version of the model revealed that we should not have excluded a simple sperm lottery as a possible mechanism of sperm competition in decorated crickets, Gryllodes sigillatus.

Measuring the sperm competition successes of field males of the yellow dung fly

Abstract 1. Sperm competition is extremely common in many species but conclusions about the relative successes of males, measured as the proportion of a female's offspring fertilised by the second male to mate with it, are based largely on laboratory studies using two laboratory‐bred males or on interrupted last copulations.2. A study was conducted in which virgin female yellow dung flies Scathophaga stercoraria mated uninterrupted with two field‐captured males.3. The results confirmed two previous conclusions: the proportion of a female's offspring fertilised by the second male was related strongly to the copula duration of the second male, and the proportion of a female's offspring fertilised by the second male was lower in larger females, though this effect was weak.4. The results indicate that previous experiments on laboratory populations of this species are likely to be relevant to wild situations, but researchers are urged to conduct studies that will improve the confidence with which laboratory measures of the proportion of a female's offspring fertilised by the second male can be assumed to reflect the sperm precedence of the last male to mate in natural situations.