Males mate with females even after sperm depletion in the two-spotted spider mite

Generally, males increase their reproductive success by mating with as many females as possible, whereas females increase their reproductive success by choosing males who provide more direct and indirect benefits. The difference in reproductive strategy between the sexes creates intense competition among males for access to females, therefore males spend much energy and time for competition with rival males for their reproduction. However, if they do not need to engage themselves into male competition and females are in no short supply, how many females can a male mate with and fertilize? We address this question in the two-spotted spider mite, Tetranychus urticae Koch. In this study, we investigated how many females a young, virgin male mated in 3 h, and checked whether the mated females were fertilized. We found that on average males mated with 12–13 females (range: 5–25). As latency to next mating did not change with the number of matings, the males are predicted to engage in even more matings if the mating trial were continued beyond 3 h. Copulation durations decreased with the number of matings and typically after 11 copulations with females any further copulations did not lead to fertilization, suggesting that males continued to mate with females even after sperm depletion. We discuss why spider mite males continue to display mating and copulation behaviour even after their sperm is depleted.

     

Possible ecological consequences of heterospecific mating behavior in two tetranychid mites

Interspecific mating between the two-spotted spider mite,Tetranychus urticae Koch, and the Banks grass mite,Oligonychus pratensis (Banks), was documented using laboratory populations. The incidence of mating betweenT. urticae males andO. pratensis females was 26.0%, while that for the reciprocal mating was 18.8%. The incidence of mating was affected by both male and female species. Such matings may have several important ecological consequences. Interspecific matings resulted in all-male progenies. Thus, progeny sex ratios may be distorted by misdirected mating behavior. In addition, heterospecific mating resulted in lower fecundity than conspecific matings in the two-spotted spider mite, although not in the Banks grass mite. Aerial dispersal behavior of the two-spotted spider mite was also affected. Under crowded conditions and deteriorating resource quality, female mites exhibit an aerial dispersal posture that helps them to become airborne, and allows them to disperse long distances. Forty-two percent ofT. urticae females that mated with conspecific males exhibited this dispersal behavior, compared to only 3.6% for virgin females. The incidence of aerial dispersal behavior for females that mated with heterospecific males was intermediate (27.3%). The effects of these behavioral alterations on male and female fitness may depend on the population structure and resource distribution.     

Age‐dependent male mating tactics in a spider mite—A life‐history perspective

Males often fight with rival males for access to females. However, some males display nonfighting tactics such as sneaking, satellite behavior, or female mimicking. When these mating tactics comprise a conditional strategy, they are often thought to be explained by resource holding potential (RHP), that is, nonfighting tactics are displayed by less competitive males who are more likely to lose a fight. The alternative mating tactics, however, can also be explained by life‐history theory, which predicts that young males avoid fighting, regardless of their RHP, if it pays off to wait for future reproduction. Here, we test whether the sneaking tactic displayed by young males of the two‐spotted spider mite can be explained by life‐history theory. We tested whether young sneaker males survive longer than young fighter males after a bout of mild or strong competition with old fighter males. We also investigated whether old males have a more protective outer skin—a possible proxy for RHP—by measuring cuticle hardness and elasticity using nanoindentation. We found that young sneaker males survived longer than young fighter males after mild male competition. This difference was not found after strong male competition, which suggests that induction of sneaking tactic is affected by male density. Hardness and elasticity of the skin did not vary with male age. Given that earlier work could also not detect morphometric differences between fighter and sneaker males, we conclude that there is no apparent increase in RHP with age in the mite and age‐dependent male mating tactics in the mite can be explained only by life‐history theory. Because it is likely that fighting incurs a survival cost, age‐dependent alternative mating tactics may be explained by life‐history theory in many species when reproduction of old males is a significant factor in fitness.     

The relative costs and benefits of territorial defense and the two conditional male mating tactics in the Comanche Springs pupfish (Cyprinodon elegans)

We examined the aggressive costs and reproductive benefits of territorial defense and its alternatives in a population of the Comanche Springs pupfish (Cyprinodon elegans). The breeding system was characterized by three different male mating tactics: territorial defense, satellite positioning, and sneak spawning. The mating tactic adopted by males reflected the males' sizes. Territorial residents were the largest, satellites were medium-sized, and sneakers were the smallest adult males observed. Consistent with the hypothesis that primary mating tactics are relatively high-cost, high-benefit strategies, we found that territorial males engaged in a number of aggressive encounters but had higher reproductive successes than any other males. However, our observations did not support the premise that conditionally breeding males engage in relatively low-benefit, low-cost tactics. Medium satellites and small sneakers acquired fewer spawns than did territorial males, but both satellites and sneakers were involved in as much aggression as territorials. That is, the data supported the prediction that satellite or sneaker males with the inability to compete for territories would attempt to accrue some reproductive opportunities in the presence of territorial males despite the high costs of spending time on the breeding grounds. Adopting conditional tactics appeared to allow satellites and sneakers to make the best of a bad situation. During a subsequent breeding season, large males were absent from the population, and medium-sized males established territories. The aggressive behavior exhibited by medium residents was similar to the previous year, but these males did not acquire higher reproductive successes than medium satellites had. The implications of switching tactics and the influence of operational sex ratios on the costs and benefits of the male tactics are briefly addressed. Electronic Publication     

Sex, drugs and mating role: testosterone-induced phenotype-switching in Galapagos marine iguanas

Males of many vertebrate species have flexible reproductivephenotypes and must decide before each mating season whetherto adopt sneaker, satellite, or territorial mating tactics.How do males gauge their abilities against others in the population?We tested experimentally whether hormone–behavior feedbackloops allow Galapagos marine iguana males to activate theirthree behavioral phenotypes as predicted by the relative plasticityhypothesis. Territorial males defended small mating areas andhad significantly higher plasma testosterone (T) levels (75± 11 ng/ml) than did satellite males that roamed aroundterritories (64 ± 8 ng/ml) or sneaker males that behavedlike females within territories (43 ± 11ng/ml). In territorialmales, temporary pharmacological blockade of T slowed head-bobpatrolling, decreased territory size threefold, and reducedthe number of females on territories 20-fold. This supportsprevious data that females may gauge male attractiveness byusing head-bob patrolling, here shown to be a T-dependent trait.Control-treated neighbors reacted to the weakening of T-blockedmales by increasing head-bob rate fivefold and territory size1.6-fold, and female numbers increased 2.5-fold. Unmanipulatedor control-injected males remained unchanged. Behavioral effectswere partly reversed after 7 days. T injections induced satellitemales to establish temporary territories, even at unconventionallocations. Some T-boosted satellite males suffered serious fightinginjuries. T-injected sneakers left female clusters and behavedlike larger satellite males that roam around territories. Thus,territorial and mating tactics are activated by T, but experimental(de-) activation at the wrong ontogenetic stage is costly: manipulatedmales switched phenotype but thereby lowered their access tofemales. We hypothesize that T levels of males that are basedon early-season behavioral interactions influence a males' subsequentphenotypic role.     

Reproductive Success Associated with Territoriality, Sneaking, and Grouping in Male Rose Bitterlings, Rhodeus ocellatus (Pisces: Cyprinidae)

The spawning success of male rose bitterlings, Rhodeus ocellatus, adopting an alternative reproductive style, was estimated through behavioural data and electrophoretic paternal analyses in field observations and experiments. Three mating patterns were observed: territoriality, sneaking, and grouping. Mating patterns depended on a male's relative size and on local male density (the number of males around a spawning spot: a mussel). Spawning patterns (pair spawning, pair spawning with sneaker, and group spawning) varied with local male density. Time-budget data of the territorial males indicated a trade-off between chasing and courtship behaviour as local male density changed. Females deposited appoximately only 1 egg per egg-laying into the mussels. As a result of isozyme analysis, a minimum of 12% (two out of 17) of the offspring in the sample were found to have been fathered by sneaker males in pair spawning with sneaker. I scored through behavioural data the mating success per spawning for each pattern, on an individual basis. The average reproductive success per spawning for each pattern was: territorial (0.61), sneaking (0.31) and grouping (0.11), and thus the successes of the patterns were not equal. Accordingly, the alternative reproductive styles of male rose bitterlings are best interpreted as alternative phenotypes in a conditional behaviour.     

Mate-guarding in a promiscuous insect: species discrimination influences context-dependent behaviour

Mating strategy is often informed by social context. However, information on social environment may be sensitive to interference by nearby heterospecifics, a process known as reproductive interference (RI). When heterospecific individuals are present in the environment, failures in species discrimination can lead to sub-optimal mating behaviours, such as misplaced courtship, misplaced rivalry behaviours, or heterospecific copulation attempts. All aspects of mating behaviour that are influenced by social context may be prone to RI, including copulatory behaviours associated with mate-guarding in the presence of possible competitors. Here we investigate the effect of three heterospecifics on the mate-guarding behaviour of male Lygaeus equestris seed bugs. We find that, despite previously reported heterospecific mating harassment amongst these species of lygaeid bug, male L. equestris are able to effectively distinguish rival conspecific males from heterospecifics. Thus, heterospecific mating attempts in this group may reflect selection on males to mate opportunistically, rather than a failure of species discrimination.     

Me against who? Male guppies adjust mating behaviour according to their rival’s presence and attractiveness

Sexual selection theory suggests that males need to constantly reappraise their mating decisions to take account of the presence and the phenotypes of their rivals. Here we examine this expectation by asking: (i) If the presence of a rival influences male mating behaviour; (ii) How important is the attractiveness of the rival (absolute attractiveness) in shaping male behaviour; and (iii) How does a male's attractiveness in comparison to his rival (relative attractiveness) influence a male's mating decisions. Using the Trinidadian guppy, a species in which female mate choice (based on males’ attractive traits) plays an important role in male mating outcomes, we recorded the frequency of courtship displays and unsolicited attempts by focal males. First, we quantified focal male mating behaviour with and without a rival. Since the probability of a successful mating is, on average, halved by the presence of a rival, we predicted that under competition the focal male would invest more in less costly mating tactic—unsolicited attempts. Second, we examined how the rival's standard length and area of orange coloration mediated focal male mating behaviour. We found that rival presence influenced how focal males responded to females in terms of both mating tactics. However, the rival attractiveness elicited changes only in male courtship display. Focal males increased courtship display rate if his rival was small or if possessed large amounts of orange, regardless of considering rival absolute or relative attractiveness. Our results show that males invest in the costlier mating tactic when there is no rival or in the presence of a smaller rival. Interestingly, they make a similar investment in the presence of an attractive orange rival. Overall, this study highlights the importance of fine‐grained male decisions in mating encounters and shows that mating tactics are differentially shaped by multiple competition risk cues.     

Seasonal dynamics of agonistic displays in territorial and non-territorial males of goitered gazelle

Aggression serves a great variety of social functions, one of which is protection of individual territories from intruders. Territorial males of many antelope species show aggressive noncontact displays, and only rarely fight. It has been suggested that ungulate males tend to have more frequent and longer aggressive interactions with rivals of similar age or social status than with males of dissimilar status. In the present paper, we test whether territorial and non-territorial males behave in a similar manner and avoid fights, and whether or not they preferentially direct aggressive and longer agonistic interactions towards males of similar age or social status, rather than towards other classes of males. We found that territorial males usually avoided straight fights with peers, and instead mainly used noncontact displays in aggressive interactions. In contrast, non-territorial males used fights considerably more often, especially during the onset of territoriality in April to May, when these males had their most frequent aggressive interactions. Territorial bucks aggressively interacted most frequently with non-territorial males and significantly less often with other territorial males, but agonistic noncontact displays between territorial males lasted the longest. In contrast, non-territorial males addressed their aggressive noncontact displays and fights most often to peers and less frequently to sub-adults. Asymmetry in the social status of territorial vs. non-territorial males was likely responsible for the distinctively different agonistic behaviors shown by the two types of males, which in turn are likely due to the different costs and benefits each male can accrue from these aggressive interactions.     

Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika

Telmatochromis vittatus (Cichlidae) is a Tanganyikan substrate brooder which spawns in the gastropod-shell nests of a cichlid, Lamprologus callipterus. We describe male reproductive tactics of T. vittatus in and around the shell nests, where males of various sizes were found. Based on utilization patterns of the shell nests, interactions among males, and spawning behaviors, males could be categorized into four types based on reproductive tactics and in order of body size: sneaker males, satellite males, territorial males and piracy males. Size range of males in tactic groups rarely overlapped. Territorial males defended shell nests harboring multiple females, but during pair-spawning they were occasionally taken over by large piracy males that visited several nests repeatedly. Small sneaker males darted to pair-spawning territorial males and might ejaculate sperm. Satellite males did not perform parasitic spawning but pair-spawned in a single shell outside the nests. Spawning of satellite males was infrequently parasitized. The largest gonado-somatic index (GSI) was found in sneaker males followed by piracy males, territorial males and satellite males, suggesting that gonadal investment of males using the four tactics may be consistent with intensity or risk of sperm competition.     

The mating system of a bee fly (Diptera: Bombyliidae). II. Factors affecting male territorial and mating success

Males of an undescribed bombyliidfly (Comptosia sp.)occupy traditional territories on a Southeast Queensland hilltop, to which females come solely for the purpose of mating. Territorial fights between males involve aerial collisions during which modified spines on the wing margins produce scars on the bodies of opponents. Territory owners and mating males are not different in size or age from the remainder of the male population. Although residency is related to fighting success, the strength of the effect is ambiguous. Consequently, our data do not appear to fit predictions from game theoretical models for fighting protocol. Hilltop males lacked the extensive population variation typically found in territorial species, and thus, the presumed advantages of traits such as large size may be suppressed. Hilltop males were larger than males at a nonhilltop, resource-based mating site and the possibility of alternative mating tactics is discussed.     

Pre-oviposition Ejaculation in Externally Fertilizing Fish: How Sneaker Male Rose Bitterlings Contrive to Mate

Pre-oviposition ejaculation as a mating tactic of sneaker males in the rose bitterling, Rhodeus ocellatus, was studied under natural and artificial conditions. In a small pond in Yao city, Osaka, Japan, the operational sex ratio of males and females was found to be approximately 3.5:1 and the proportion of males to the mussels, which serve as spawning beds for the rose bitterling, was approximately 2:1. Competitively subordinate rose bitterling males which spawned into the mussels participated in mating by sneaking, because not all males could occupy territories around the mussels. The sneaker males often released sperm not only after but also before egg-laying (this ejaculation movement by the male before egg-laying is termed ‘pre-oviposition ejaculation’). In pair spawning with sneaker, the sneakers frequently performed pre-oviposition ejaculations, which territorial males never performed. In the field, pre-oviposition ejaculations by sneakers coincided with the leading of females by territorial males. Under artificial conditions, I demonstrated by using electrophoretic paternal analyses that the pre-oviposition ejaculations by the sneakers were more effective than the post-oviposition ejaculations by the territorial males. In addition, there were negative size-dependences in ejaculation achievement rate and fertilization success of the sneaker males.     

Mating tactics and male-male courtship in the lek-breeding cichlid Oreochromis mossambicus

Data are presented on the breeding behaviour of Oreochromis mossambicus under captive conditions. Males tended to synchronize their occupation of territories and breeding activities. Different male mating tactics were observed, namely establishing a breeding territory, acting as a floater, or behaving as a sneaker. The majority of spawnings observed involved dominant males and were subjected to interference from other males. Males were found to court other males that frequently responded to these attempts by adopting a female-like behaviour. Results are discussed in terms of a probable time constraint in territoriality, which promotes male-male competition and a low level of sex discrimination by territorial fish.     

Size Dependent Male Reproductive Tactic in the Two-Spotted Goby (Gobiusculus flavescens)

Male investment in testes and sperm duct gland in the polygamous nest breeding two-spotted goby Gobiusculus flavescens (Fabricius) was investigated in relation to time in reproductive season and individual physical parameters. This small teleost fish is most likely the most abundant species found along the rocky shores of the North East Atlantic. The two-spotted goby has a single reproductive season, during which nest-caring males can raise several clutches of offspring. According to the literature the males are on average larger than the females. Here we report for the first time a population showing a reversal of this trend, with males on average being smaller than females, a difference likely caused by a large proportion of small males. Early in the breeding season these small males have typical sneaker characters, with relatively large testes and small seminal duct glands compared to the larger dominant territorial males. The presence of these two alternative male reproductive tactics is confirmed by histological studies, which shows the presence of sperm in the sperm duct glands (SDG) of smaller males, but not in the SDG of intermediate and larger males. To our knowledge, males with typical sneaker characters have not been reported in earlier studied populations of two-spotted goby. Interestingly we found that testes investment declined significantly over the course of the breeding season, and that this reduction was significantly more pronounced in small compared to the large males. Further, a significant increase in seminal duct gland (SDG) mass was observed for the smaller males over the breeding season. We propose that this indicates a possible shift in mating tactic by smaller males from a parasitic to a nest-holding tactic over the course of the breeding season. Thus, the observed size dependent plasticity in investment in SDG over time suggests that the reproductive tactic of G. flavescens is conditional, and possibly influenced by mate availability and male—male competition.     

Differential grooming rate and tick load of territorial male and female impala, Aepyceros melampus

During the breeding season in Zimbabwe territorial male impalawere found to engage in much less self oral grooming and allogroomingthan females, presumably as a reflection of the need to remainvigilant in herding females and repulsing challenging bachelormales. Territorial males spent an average of 11 min engagedin all types of grooming during a 12-h day, compared with 40min grooming by females. Rutting activity and time spent scanningpeaked in May, while self oral grooming and feeding by territorialmales was lowest at this time. The decrement in grooming bymales (relative to females) represented half of all time devotedto rutting behaviors. Territorial males appeared to sacrificefeeding and grooming time in exchange for more time devotedto vigilant activities essential to mating success. In a comparableregion of Zimbabwe, territorial males were also found to harborabout six times as many adult ticks as the females on the sameterritories during the breeding season. Because grooming isunderstood to be effective in removing ticks, the higher tickload of territorial males was attributed to their reduced groomingbehavior. However, testosterone and adrenal cortical steroids,which are elevated in territorial male impala, are known todepress the immune system, and so may be important in controllingparasite infections. Sexually active males of many species aregenerally found to harbor more parasites than females. The differencein tick load between territorial male and female impala mayreflect both behavioral and hormonal parameters.     

The adaptive significance of non-contact mate guarding by males of the dragonfly,Nannophya pygmaea Rambur (Odonata: Libellulidae)

InNannophya pygmaea, ovipositing females were frequently disturbed by conspecific males. Disturbed females often copulated with one of these males or flew away from the pool. Females which flew away from the pool due to male disturbance often returned later the same day and mated with different males. A territorial male would guard his ovipositing mate by hovering above her, presumably trying to prevent her from moving out of his territory. A non-territorial male would also guard his mate in a similar way, both at a vacant water area which was not occupied by any territorial males, or within the territory of a resident male. In addition, both territorial and non-territorial males chased intruding males in an attempt to prevent their mates from being stolen. Territorial males defended their mates better than non-territorial males. Both males and females often mated more than once in the course of a single day. Some territorial males copulated with a new female while another mate oviposited in their territories. This observation supported the “multiple mating hypothesis” proposed by Alcock (1979) and Uéda (1979) but other evidence suggested that this is an inadequate explanation for the non-contact guarding ofN. pygmaea.     

Asymmetry in male lethal fight between parapatric forms of a social spider mite

Closely related species often show adjacent geographic distributions, albeit with some overlap. This contiguity is thought to result from secondary contact between (spatially separated) diverging groups or from parapatric speciation. Fights between males of closely related species will affect their chance to mate with females of the other species, which in turn may promote their spatial segregation and drive their speciation. Stigmaeopsis miscanthi is a social spider mite that lives in a group within self-woven nests on leaves of Chinese silver grass. This mite shows lethal male–male fight as a means to maintain a harem, and has two forms showing differences in the levels of male–male aggression, diapause intensity in females and the relative length of the first to third legs. The two forms show parapatric distributions. We found that males of one form readily engage themselves in lethal fight with males of the other form, thereby acquiring the nests and gaining access to females of this other form. Males of the aggressive form tend to win the fights with males of the other form. Their first legs are longer which may provide them with a better weapon and which also indicate a larger body width. However, another determinant of who wins the fight is the length of the third legs which can be a proxy for body length. Based on these results, we hypothesize that male killing behavior is one of the mechanisms maintaining parapatry (instead of sympatry) of the two spider mite forms apart from difference in diapause attributes.     

Effects of Social Structure on the Behaviour and Performance of Alternative Reproductive Phenotypes in Male Rock Shrimp, Rhynchocinetes typus

Males that adopt alternative mating tactics within a conditional strategy often undergo costly morphological changes when switching to the next phenotype during ontogeny. Whether costs of changing to a subsequent reproductive phenotype are outweighed by a higher mating probability may depend on the frequencies of different phenotypes in a group of competitors. Benefits and costs associated with different phenotype frequencies depend on interactions within and between alternative phenotypes, but the underlying behavioural mechanisms have rarely been studied. Herein, we used the rock shrimp Rhynchocinetes typus as a model: ontogenetic male stages of this species differ in morphological and behavioural traits that indicate alternative reproductive phenotypes. The small, subordinate, male stage (typus) develops via several intermediate stages (intermedius) to the dominant male stage (robustus): in competitive interactions the typus males usually employ the sneaking tactic, while the robustus males invariably employ the monopolizing fighter tactic. In laboratory experiments, we manipulated phenotype frequencies to examine whether there are frequency‐dependent effects on searching behaviour, aggressiveness and mating probability. With increasing frequency of robustus males, the rate of aggressive interactions among them increased. Furthermore, robustus males increased walking velocity when more than one robustus male was present. In contrast, typus males did not adjust their searching or aggressive behaviour. The increase of aggressive interactions among robustus males provided more opportunities for typus males to seize a temporarily unguarded female. While typus males exploit fights among robustus males that produce mating opportunities for them, robustus males benefit from typus males, which reveal the presence of receptive females. We suggest that each phenotype benefits from the presence of the other phenotype and suffers costly interference among individuals of the same phenotype. Whether frequency‐dependent effects on the mating probability of subordinates also affect their ontogenetic switchpoint should be examined in future studies.     

Territoriality in the green frog (Rana clamitans): Vocalizations and agonistic behaviour

Territorial behaviour of Rana clamitans was studied in an experimental pond containing natural vegetation and artificial shelters. Males defended territories from June through August. Five vocalizations were used in territorial advertisement and agonistic encounters. Agonistic behaviour included patrolling, splashing displays, chases, attacks and wrestling. About 23% of all encounters ended in wrestling bouts. Most bouts were less than 30 s long, but some lasted up to 45 min. Most fights were won by residents. Intruders were most successful in fights when they were larger than residents or previously had been residents of other territories. Weight loss by large males enabled some smaller males to oust residents from territories. Possible costs of fighting include energetic costs and exposure to predation. Large male body size in R. clamitans and other territorial frogs may be an adaptation for fighting.