Sex-specific spawning behavior and its consequences in an external fertilizer

Identifying the target of sexual selection in externally fertilizing taxa has been problematic because species in these taxa often lack sexual dimorphism. However, these species often show sex differences in spawning behavior; males spawn before females. I investigated the consequences of spawning order and time intervals between male and female spawning in two field experiments. The first involved releasing one female sea urchin's eggs and one or two males' sperm in discrete puffs from syringes; the second involved inducing males to spawn at different intervals in situ within a population of spawning females. In both, fertilization success was measured as the fraction of eggs fertilized and the paternity share of each male. The results indicate that spawning after females imposes a cost on males but only during sperm competition. Further, the optimal interval between the initiations of male and female spawning depends on degree of sperm competition, distance between males and females, and water velocity. The results show that sex differences in spawning timing of marine invertebrates can be explained on the basis of the differential costs and benefits of spawning out of synchrony with the other sex and that the result of sexual selection on external fertilizers may be behavioral rather than morphological differentiation of the sexes.     

Secondary sexual characters and sperm traits in coho salmon Oncorhynchus kisutch

A study was undertaken to examine secondary sexual characters (spawning colouration and overall body size) in relation to sperm metrics in one alternative reproductive tactic of coho salmon Oncorhynchus kisutch : large hooknose males that spawn in dominance-based hierarchies. Males with less intense red spawning colouration had higher sperm velocities than males with darker red spawning colouration. There was no relationship between male body size and sperm metrics. These results suggest that within an alternative reproductive tactic, variation in sperm competition intensity may select for a trade-off between investment in sexual colouration and sperm quality.     

Ejaculate expenditure by malebush crickets decreases with sperm competition intensity

Male bushcrickets transfer a spermatophore at mating that consists of a sperm-containing ampulla and a sperm-free mass, the spermatophylax, that is consumed by the female during insemination. The costs of spermatophore production for males and benefits of consumption for females result in reversals in courtship roles in nutrient limited populations that increase both the risk and intensity of sperm competition. Here we show that under conditions characteristic of courtship role reversal, male expenditure on the spermatophore is dependent on female size. When mating with small females, males increase the amount of spermatophylax material and sperm, as expected from the increased sperm competition risk associated with courtship role reversal. However, males reduce the amount of spermatophylax material and sperm transferred to larger females. Since larger females have a higher mating success when competing for nurturant males, the intensity of sperm competition covaries with female size. Reduced ejaculate expenditure under increased sperm competition intensity is in accord with theoretical expectation.     

Male crickets adjust the viability of their sperm in response to female mating status

Sperm competition theory predicts that males should allocate sperm according to the number of competing ejaculates. Prudent allocation of sperm in response to different levels of sperm competition has been found across a number of taxa; however, some studies suggest that males may not always allocate sperm as expected. Here we examine sperm allocation in the Australian field cricket Teleogryllus oceanicus, using female mating status (virgin, singly mated, or multiply mated) to manipulate male perception of sperm competition risk and intensity. Consistent with theory, we found that male crickets adjust their ejaculates in response to female mating status. However, rather than altering the absolute numbers of sperm transferred to a female, males altered the quality of their sperm. Males ejaculated sperm of low viability (proportion of live vs. dead sperm) when mating with virgins, increased sperm viability when mating with singly mated females, but reduced sperm viability when mating with multiply mated females. Our results show that variation in ejaculate quality can be an important aspect of strategic ejaculation by males and suggest caution in the interpretation of studies in which males do not appear to allocate sperm according to theory.     

Spawning behavior of Arctic charr (Salvelinus alpinus): Spawning synchrony,vibrational communication,and mate guarding

A mismatch in synchrony between male and female gamete release in external fertilizers can result in reduced or failed fertilization, sperm competition, and reduced paternity. In Arctic charr (Salvelinus alpinus), males can adopt either a guard or sneak tactic resulting in both pre‐ and postcopulatory competition between males with alternative reproduction tactics. Here, spawning behavior of free‐living Arctic charr was video‐recorded, and their reproductive behavior was analyzed. From evaluating 157 spawning events, we observed that females mainly spawned with a guarding male and that the female and the guarding male synchronized timing of gamete release under sperm competition. Although sneakers spawned with higher synchrony than the guarding male in single‐male spawning events, the average sneaker released his milt less synchronized with the female than the guarding male under sperm competition. Approximately 50% of the recorded spawning events occurred under sperm competition, where each event included an average of 2.7 males. Additionally, sneakers were more exposed to sperm competition than guarding males. An influx of males, in close proximity to the female, occurred during the behavioral sequences leading up to egg release, but this influx seemed not dependent on egg release, suggesting that something else than gonadal product attracts sneaker males to the spawning female. Just before and during the actual release of gametes, the spawning couple vibrates their bodies in close contact and it seems likely that this vibrational communication between the spawning couple, which results in a larger amplitude sound wave than seen under regular courting, reveals time of gamete release to sneaker males. Thus, vibrational communication may enable synchrony between the guarding male and the female, and this might be traded against the cost of higher detectability from surrounding sneaker males, eavesdropping in close proximity.     

Male sperm expenditure under sperm competition risk and intensity in quacking frogs

In the frog Crinia georgiana, reproductive behavior comprisesa "guarding tactic," in which males defend spawn sites and attractfemales by calling, and a "sneak tactic," in which males joinspawning pairs. The aims of the present study were to (1) relateejaculate expenditure by "guarding" and "sneak" males to theirprobability of mating with other males present (sperm-competitionrisk), and (2) determine if males adjust their ejaculate expenditureaccording to the number of males involved in a spawning (sperm-competitionintensity). Theory predicts that because sneak males alwaysmate with other males present, they will experience a highersperm-competition risk and should release larger ejaculatesrelative to that of guarding males. However, as the proportionof sneaks in a population increases so does the risk of spermcompetition to guarders, so expenditure by each tactic shouldmove toward equality. Given that the incidence of sneak behavioris high in C. georgiana, guarders and sneaks were expected toexperience similar risks of sperm competition and show similarinvestment in spermatogenesis. Comparison of testes size andejaculate size showed no difference between tactics. Modelsof sperm-competition intensity predict that males should increasetheir ejaculate size when spawning in the presence of one othermale but decrease their ejaculate size when spawning in thepresence of multiple males. Here, males maintained a constantsperm number irrespective of whether a mating involved one,two, or three males. This result suggests that male C. georgianado not facultatively adjust ejaculate investment in responseto fluctuating intensities of sperm competition.     

The importance of sperm competition risk and nest appearance for male behavior and female choice in the sand goby, Pomatoschistus minutus

To test if an increased sperm competition risk affects malebehavior and mating decisions of both sexes, we performed twoexperiments using the sand goby, Pomatoschistus minutus, a nest-buildingfish with exclusive paternal care. In our first experiment,a nest-holding male, with a confined female, was sequentiallyexposed to a vial with a sneaker male or an empty vial. Whilemale courtship, nest building, displacement fanning, and timeoutside the nest were unaffected, individual males showed ahigher mucus preparation effort inside the nest in the presenceof a sneaker male than when alone. We found such mucus to containsperm, thus clearly suggesting an importance in sperm competition.In our second experiment, a female was free to spawn with twodifferent males, one of which was exposed to a confined sneakermale. Male mating success was not affected by the presence ofa sneaker male. However, the volume of sand the male had puton his nest was positively associated with female spawning decision,while nest-opening width was not. In a partial correlation offive traits thought to attract females (nest-opening width,sand volume, male courtship display, displacement fanning, andmale size), males that fanned well were found to also buildlarge nests or display intensely, but not both. This indicatesthat rather than being jacks-of-all-trades, individual malesfocus on a subset of traits for attracting females.     

The effect of alternative mating tactics on the fertilization success of a hermaphroditic seabass

In the simultaneously hermaphroditic marine fish, Serranus subligarius, male role individuals are known to pair spawn, group spawn and streak spawn. While the effects of these common mating tactics on mating success in the male role have been well studied, their consequences for the reproductive success of the individuals taking the female role have received little attention. To investigate those consequences, I observed mating behaviors and quantified fertilization success in natural and experimental settings during the summers of 2005-2008 at three sites with different local population densities. I observed focal individuals in 15-min increments and recorded the total number of spawns, number of streak spawns, size of participating spawners, and fertilization rate. The occurrence of small-sized individuals in the local population is associated with higher frequencies of streaking behavior; these small fish are most often first-year individuals reaching sexual maturity late in the spawning season (August/September). Spawns that included one or more streak spawners had a significantly lower average fertilization rate (89?%) than pair spawns without a streak spawner (97?%). This pattern was confirmed with a field manipulation experiment in which spawning events that included streakers again showed lower fertilization rates (93?%) than spawning events that did not include streakers (98?%). These lower fertilization rates occurred despite the fact that spawns that included multiple males produced, on average, 20?% more sperm than produced in spawns with only a single male. These results indicate that females incur a significant fitness cost when streakers invade a spawning event, a cost not attributable to sperm limitation or any direct effects on the female.     

Competitive mate searching in male common toads, Bufo bufo

The reproductive behaviour of a population of individually marked toads Bufo bufo was studied at a pond where males outnumbered females by between four and five to one. There was intense competition between the males for mates and only 20·5 % of them bred successfully. Of the successful males, 38·5 % got mates by fighting and displacing other males from the backs of females (takeovers). Larger males enjoyed greater reproductive success because they were stronger and better able to achieve takeovers. When competing for females, some males searched at the spawn site while others searched away from spawn. The numbers searching in the two areas can be predicted by a model which assumes that unpaired males distribute themselves so that there is a spatial ESS, where individuals have equal expectations of finding a female both at and away from the spawning ground.     

Operational sex ratio and resource defence as predictors of the mating system in European bitterling

Operational sex ratio (OSR), the ratio of sexually active males to fertilizable females in a population, plays a central role in the theory of mating systems by predicting that the intensity of male–male competition and the degree of sexual selection increases as the OSR becomes increasingly male biased. At high values of OSR, however, resource defence theory predicts the breakdown of territoriality and a shift towards scramble competition with a decrease in sexual selection. The direction that correlations between OSR and resource competition and variance in mating success will take depends on the biology of the species of interest. We investigated the effects of male population density and male‐biased operational sex ratio on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus . This species spawns inside living unioneid mussels. Large males defended territories, were aggressive towards conspecifics under equal sex ratios and monopolized pair spawnings with females. The mating tactic, however, changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. This change in male behaviour from pair to group spawning has two ramifications for sexual selection. The intensity of sexual selection and variance in male mating success decrease, and the form of sexual competition changes from resource‐ to sperm competition. Thus, the use of alternative mating tactics renders the OSR unable to predict the direction of resource competition and variance in male mating success at high densities.     

Butterflies tailor their ejaculate in response to sperm competition risk and intensity

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 of 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 butterfly 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 affecting sperm competition risk, tailoring their ejaculates as predicted by recent theoretical models.     

Male scorpionflies assess the amount of rival sperm transferred by females' previous mates

Theory predicts that when sperm compete numerically, selection will favor males who vary the number of sperm they transfer with the immediate level of sperm competition. In this study, I measured male mating investment in response to both female mating status (virgin vs. mated) and the number of foreign sperm stored by females in a previous mating in the scorpionfly Panorpa cognata. Female sperm storage was manipulated by interrupting copulations at different time points. Female mating status did not significantly influence male mating investment, but resource-limited males invested strategically in relation to the amount of sperm stored by females in a previous mating. I found continuously decreasing male investment in response to increasing amounts of competing sperm. These results demonstrate an unprecedented male ability to assess the number of sperm stored by females. As a result, males are capable of an extraordinarily fine-tuned reaction to the intensity of sperm competition.     

Assessing the potential for post‐ejaculatory female choice in a polyandrous beach‐spawning fish

In species with limited opportunities for pre‐ejaculatory sexual selection (behavioural components), post‐ejaculatory mechanisms may provide opportunities for mate choice after gametes have been released. Recent evidence from a range of taxa has revealed that cryptic female choice (i.e., female‐mediated differential fertilization bias), through chemical cues released with or from eggs, can differentially regulate the swimming characteristics of sperm from various males and ultimately determine male fertilization success under sperm competition. We assessed the potential role that such female‐modulated chemical cues play in influencing sperm swimming characteristics in beach‐spawning capelin (Mallotus villosus), an externally fertilizing fish that mates as couples (one male and one female) or threesomes (two males and one female) with presumably limited opportunities for pre‐ejaculatory sexual selection. We assayed sperm swimming characteristics under varying doses and donor origins of egg cues and also examined the possibility of assortative mating based on body size. We found mating groups were not associated by size, larger males did not produce better quality ejaculates, and egg cues (regardless of dosage or donor identity) did not influence sperm swimming characteristics. Our findings suggest that intersexual pre‐ejaculatory sexual selection and cryptic female choice mediated by female chemical cues are poorly developed in capelin, possibly due to unique natural selection constraints on reproduction.     

Sperm competition games: optimal sperm allocation in response to the size of competing ejaculates

Sperm competition theory predicts that when males are certain of sperm competition, they should decrease sperm investment in matings with an increasing number of competing ejaculates. How males should allocate sperm when competing with differently sized ejaculates, however, has not yet been examined. Here, we report the outcomes of two models assuming variation in males' sperm reserves and males being faced with different amounts of competing sperm. In the first 'spawning model', two males compete instantaneously and both are able to assess the sperm competitive ability of each other. In the second 'sperm storage model', males are sequentially confronted with situations involving different levels of sperm competition, for instance different amounts of sperm already stored by the female mating partner. In both of the models, we found that optimal sperm allocation will strongly depend on the size of the male's sperm reserve. Males should always invest maximally in competition with other males that are equally strong competitors. That is, for males with small sperm reserves, our model predicts a negative correlation between sperm allocation and sperm competition intensity, whereas for males with large sperm reserves, this correlation is predicted to be positive.     

Reproductive behaviour of the filefishRudarius ercodes: male spawning parades and female choice

Synopsis The reproductive behaviour ofRudarius ercodes is described from undersea observations in Aburatsubo Bay, Japan. Reproductive behaviour can be separated into four parts: (1) Prespawning Search = searching for spawning sites by females and searching for gravid females by males, (2) Spawning Parade = males follow a gravid female in a line, competing with each other to reach the head of the queue, (3) Spawning = the female takes the spawning position, males rush to the side of the female, and mating occurs between one female and several anterior males of the spawning parade, (4) Parental Care = females attach adhesive eggs to seaweed with the mouth and guard them until embryos hatch. There is no male parental care. The reproductive season ranges from May to October and spawning occurs early in the morning every day. Females begin feeding early in the morning, but males feed little at this time.R. ercodes shows neither territorial behaviour nor fixed-pair spawning. One male might spawn several times in one morning. One female spawns at most once every 5 days. The mating system of this species is promiscuous. The probable function of the spawning parade as a style allowing female choice is discussed.     

Paternity in horseshoe crabs when spawning in multiple-male groups

Unpaired or satellite male horseshoe crabs, Limulus polyphemus, are attracted to and often form a group around a pair (a female with an attached male) that is nesting in the high intertidal zone. These males are engaged in sperm competition. We observed nesting pairs and their associated satellites in the wild, collected and reared their eggs and used genetic markers to examine paternity. We found that the unpaired, satellite males are highly successful at fertilizing eggs; two satellites can leave the attached male with few fertilizations. Two satellites together are each as successful as one spawning with a pair. A satellite's location around the female greatly affects his success, and males compete for access to a position over the dorsal canal between the prosoma and opisthosoma of the female and under the front margin of the paired male where they are most likely to fertilize eggs. Although eggs and sperm retain their viability for some time after spawning, nearly all eggs are fertilized by the satellites that are around the nesting pair at the time of egg laying and by the attached male. A number of factors including beach current, female size and male behaviour affect the outcome of sperm competition in this externally fertilizing species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Optimal Mate Searching Strategy in the Symbiotic Spider Crab Inachus phalangium (Decapoda)

The reproductive strategy of the symbiotic spider crab, Inachus phalangium was studied from 1981 to 1983 in the natural environment. Main study focus was the efficiency of males in search of mates. I. phalangium females are site-constant, and live in the protection of one anemone or group. Males travel frequently between anemones harbouring females due to spawn; they copulate and guard the females until spawning, after which the male leaves again. A male operates in a patrol area containing 3–8 anemone groups and up to 8 females, visiting each female in turn repeatedly just before it is due to spawn. Patrol areas of different males may overlap, with resulting competition to fertilize a female's next brood. Large males have higher reproductive success than small ones. Females live up to 8 months after the moult of puberty and hatch up to six broods, and males live up to 7 months as adults. A male could fertilize a calculated 26,000 eggs, whilst a female's reproductive potential is ca. 4,200 eggs. Mortality risks are higher for males than for females, probably because of increased predation while leaving the protection of anemones in order to visit females. Males learn the positions of anemones harbouring females in their patrol areas, and when these are due to spawn. This allows a male to travel with a target and arrive punctually to fertilize the next brood due in his circuit. I. phalangium is the first marine invertebrate reported to use a “schedule” of localities and times for visiting prespawning females. In this way males minimize searching time and mortality risk, and maximize the number of broods fertilized.     

Reproductive-tactic-specific variation in sperm swimming speeds in a shell-brooding cichlid

Theory predicts that males experiencing elevated levels of sperm competition will invest more in gonads and produce faster-swimming sperm. Although there is ample evidence in support of the first prediction, few studies have examined sperm swimming speed in relation to sperm competition. In this study, we tested these predictions from sperm competition theory by examining sperm characteristics in Telmatochromis vittatus, a small shell-brooding cichlid fish endemic to Lake Tanganyika. Males exhibit four different reproductive tactics: pirate, territorial, satellite, and sneaker. Pirate males temporarily displace all other competing males from a shell nest, whereas sneaker males always release sperm in the presence of territorial and satellite males. Due to the fact that sneakers spawn in the presence of another male, sneakers face the highest levels of sperm competition and pirates the lowest, whereas satellites and territorials experience intermediate levels. In accordance with predictions, sperm from sneakers swam faster than sperm from males adopting the other reproductive tactics, whereas sperm from pirates was slowest. Interestingly, we were unable to detect any variation in sperm tail length among these reproductive tactics. Thus, sperm competition appears to have influenced sperm energetics in this species without having any influence on sperm size.     

Reproductive investment patterns,sperm characteristics,and seminal plasma physiology in alternative reproductive tactics of Chinook salmon (Oncorhynchus tshawytscha)

Although alternative reproductive tactics (ARTs) are common across a range of taxa, little is known about whether the different tactics have adapted to sperm competition risk. Chinook salmon, Oncorhynchus tshawytscha, have two ARTs: large males that participate in dominance‐based hierarchies for access to spawning females, known as hooknoses, and small males that attempt to sneak fertilizations during spawning events from peripheral positions, known as jacks. Jacks continually face sperm competition risk because they always spawn in the presence of another male, whereas hooknoses face relatively low sperm competition risk because other males are not always present during spawning events. Based on the sneak‐guard model of sperm competition this asymmetry in sperm competition risk predicts that jacks ought to invest significantly more into sperm‐related traits important for sperm competition success relative to hooknoses. In the present study we report on reproductive investment patterns, sperm characteristics, and seminal plasma physiology of males that exhibit ARTs in Chinook salmon. We found that jacks invest significantly more of their somatic tissue into gonads compared with hooknoses. Sperm velocity also varied significantly between the ARTs, with jacks having significantly faster sperm than hooknoses. No significant differences in seminal plasma physiology metrics related to sperm quality were detected between the ARTs. We interpret these sperm investment patterns in light of the sneak‐guard model of sperm competition that is based on differences in sperm competition risk and alternative investment possibilities among ARTs. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Sperm competition games between related males

Three sperm competition games against relatives are examined. In the first, a male has no information at the time of mating as to whether or not his ejaculate will face sperm competition from a related or unrelated male. Sperm expenditure increases with overall sperm competition risk q and declines with the probability rho that the competitor shares the same allele for sperm expenditure. In the second game, males have almost perfect information: they 'know' whether there will be sperm competition and, if so, whether this involves a related or unrelated male. Sperm expenditure is reduced by a factor rho when competing with a relative. In the third game, males 'know' when they compete with relatives, but have no information for other matings whether they will face sperm competition from unrelated males. A male without information expends less on his ejaculate than a male competing with a close relative if the overall risk of sperm competition is low, but more if the overall risk is high. The average relative ejaculate expenditure is the same in all three games so that, if this determines testis size, data is required only on the overall sperm competition risk, the probability of competing with a relative and the average rho in order to perform comparative analyses.