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.

     

Euseiusfinlandicus (Acari: Phytoseiidae) as a potential biocontrol agent against Tetranychus urticae (Acari: Tetranychidae): life history and feeding habits on three different types of food

Life history and reproductive parameters of the generalist predatory mite Euseius (Amblyseius) finlandicus (Oudemans) were studied in the laboratory at 25 +/- 1 degrees C, with a 16L:8D photoperiod and 60 +/- 15% RH, to investigate its response to different food sources: an eriophyid mite Aceria sp., tulip pollen Tulipa gesnerana L., and two-spotted spider mite Tetranychus urticae Koch. Total developmental time of the immature stages was the shortest on eriophyid mites, followed by pollen, and then spider mites. Fecundity was highest on pollen (43.69 eggs; 1.63 eggs/female/day), then eriophyid mites (39.73 eggs; 1.37 eggs/female/day) and lowest on spider mites (18.16 eggs; 0.80 eggs/female/day). Intrinsic rate of increase (Rm), net reproductive rate (Ro) and finite rate of increase (lambda) followed the same pattern [pollen (0.168, 27.96 and 1.183, respectively), eriophyid mites (0.153, 20.81 and 1.167), spider mites (0.110, 9.44 and 1.119)]. Mean generation time (days) was the shortest on pollen (19.90), followed by eriophyid mites (20.02), and then spider mites (20.59). Average spider mite larvae consumed by E. finlandicus during immature stages were 9.18 for males and 11.85 for females. Adult E. finlandicus females consumed an average of 166.38 spider mite protonymphs during adult stage compared to an average of 66.55 by males. The number of prey protonymphs consumed per day by females was highest in the oviposition period, lower in the pre-oviposition period and the lowest in the post-oviposition period. The eriophyid mite as a prey recorded the shortest developmental time, while pollen as food recorded the highest oviposition rate in E. finlandicus. The potential of this predator as a biocontrol agent against T. urticae is discussed.     

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.     

Mating modifies female life history in a haplodiploid spider mite

Mating usually modifies females' resource allocation pattern, often as a result of conflicts between male and female partners. Can such a switch occur even in the absence of sexual conflicts? We addressed this issue in the haplodiploid spider mite Tetranychus urticae, whose biology and population structure considerably reduce conflicts between males and females over reproductive decisions. Comparing virgin and mated females, we tested the hypothesis that mated females modify their allocation pattern so as to maximize their probability of producing daughters. Mated females produced fewer but larger eggs, resulting in an overall similar reproductive effort but an increased probability of producing daughters, since in this species larger eggs are more likely to be fertilized and thus to become female. Moreover, mated females concentrated their reproduction early in life. Again, this might be a way to produce more daughters, since sperm is more abundant early in life. For virgins, spreading reproductive investment might be a way to save resources to extend life span, thus increasing their probability of encountering a sexual partner. Females with multiple opportunities for mating produced fewer eggs and a less female-biased sex ratio than once-mated females, raising the question of why multiple mating often occurs in this species.     

Temperature and sex allocation in a spider mite

Although temperature is the most important environmental factor regulating arthropod development and reproduction, its influence on sex allocation in haplodiploid arthropods remains largely unexplored. We investigated under laboratory conditions how maternal age and temperature mediate offspring sex ratio of the spider mite Tetranychus mcdanieli (Acari: Tetranychidae). Over nine temperature regimes, female-biased sex ratios were consistently observed, varying from 57 to 87% among progeny produced over lifetime. Spider mite sex ratio was affected by maternal age: more male progeny were produced at both the beginning and the end of the female lifespan, yielding a dome shaped curvilinear relationship. This pattern of variation with age probably results from constraints on using sperm at young ages and sperm depletion or viability at older ages. We found a significant curvilinear relationship between temperature and sex ratio. The proportion of female offspring was lowest at intermediate temperatures and highest at extreme temperatures. We suggest that increased female-biased sex ratio at extreme temperatures is an evolutionary response of spider mites to deteriorating habitats as, in the Tetranychidae, females have better capacities than males to disperse and survive under harsh conditions.     

No variation for Wolbachia-induced hybrid breakdown in two populations of a spider mite

Wolbachia are cytoplasmically transmitted bacteria that infect several species of mites. In the two-spotted spider mite Tetranychus urticae Koch this symbiont can induce reproductive incompatibility. Wolbachia-induced reproductive incompatibility is observed in crosses between Wolbachia-infected (W) males and uninfected (U) females. This incompatibility is expressed in F1 broods as male-biased sex ratios, an effect called cytoplasmic incompatibility (CI). However, in the two-spotted spider mite, Wolbachia-induced reproductive incompatibility may extend to the F2: broods of virgin F1 females from U×W crosses sometimes suffer increased mortality rates. This F2 effect is called hybrid breakdown (HB). Several isofemale lines derived from mites collected from rose and cucumber plants had been previously tested for CI. Here we report on the results obtained for HB.     

Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan

Wolbachia are a group of maternally inherited bacteria that infect a wide range of arthropods. Wolbachia infections are known to result in the expression of various abnormal reproductive phenotypes, the best known being cytoplasmic incompatibility. The first systematic survey of 42 spider mite species in Japan revealed that seven species (16.7%) were infected with Wolbachia. Wolbachia in the spider mites were grouped into three subgroups in supergroup B by phylogenetic analyses of the wsp gene. Most spider mites did not show cytoplasmic incompatibility when infected males were crossed with uninfected females. However, all infected populations of Panonychus mori and Oligonychus gotohi (five and four populations, respectively) possessed modification-positive strains of Wolbachia, and the cytoplasmic incompatibility decreased egg hatchability and female ratio of the spider mites. Thus, some Wolbachia strains cause sex ratio distortion in their hosts.     

Some factors affecting reproduction and sex-ratio of the predacious mite Amblyseius deleoni (Muma and Denmark) (Acari: Phytoseiidae)

Abstract

Several factors were examined to determine their effect on the reproduction and sex ratio in the predacious mite Amblyseius deleoni (Muma and Denmark), in the laboratory. The factors investigated included multiple matings, duration of copulation, capacity of male for mating in excess of females and age of mating females and males. The factors included also, the host plant leaf texture, food deprivation during immature and adult stages, and prey (Tetranychus urticae Koch) density. The results indicated that females of A. deleoni require multiple matings to maximize their reproductive potential, also when copulation was allowed for increasing periods of time, there was a gradual increase in total egg production and oviposition period. A male showed a high reproductive ability for more than 15 days and was able to mate more than once in excess of females. Age of females has an influence on fecundity and sex ratio; old females decreased egg production and produced proportionally more male progeny compared with young females. Similarly, the highest number of eggs deposited per female A. deleoni was reported, when female mated with a young male (0-day old). In addition, males of A. deleoni (at any age) were able to inseminate the females. Results from host plant leaf texture indicated that guava leaf gave the highest reproduction rate, while the fig leaf gave the least female fecundity. Neither the reproductive rate nor the sex ratio of the progeny of females crossed by normal or experimental males had been influenced by the food deprivation during immature stages. A significant lower fecundity was recorded on female's A. deleoni when exposed to different food deprivation programmes during adult stage. The number of eggs laid by the predator female increased with increasing prey density of T. urtice to a maximum of 2.04 eggs deposited per day at a prey density of 30 protonymphs of T. urticae as a prey. As the level of prey density was increased, there was a shift in sex ratio towards an increased proportion of females.     

Cardinium symbionts cause cytoplasmic incompatibility in spider mites

Intracellular symbiotic bacteria belonging to the Cytophaga-Flavobacterium-Bacteroides lineage have recently been described and are widely distributed in arthropod species. The newly discovered bacteria, named Cardinium sp, cause the expression of various reproductive alterations in their arthropod hosts, including cytoplasmic incompatibility (CI), induction of parthenogenesis and feminization of genetic males. We detected 16S ribosomal DNA sequences similar to those of Cardinium from seven populations of five spider mite species, suggesting a broad distribution of infection of Cardinium in spider mites. To clarify the effect of Cardinium on the reproductive traits of the infected spider mites, infected mites were crossed with uninfected mites for each population. In one of the populations, Eotetranychus suginamensis, CI was induced when infected males were crossed with uninfected females. The other six populations of four species showed no reproductive abnormalities in the F(1) generation, but the possibility of CI effects in the F(2) generation remains to be tested. One species of spider mite, Tetranychus pueraricola, harbored both Cardinium and Wolbachia, but these symbionts seemed to have no effect on the reproduction of the host, even when the host was infected independently with each symbiont.     

Effect of mating frequency on fecundity and longevity of the predatory mite <Emphasis Type="Italic">Kampimodromus aberrans</Emphasis> (Acari: Phytoseiidae)

The effect of single versus multiple mating on longevity and fecundity as well as the number of matings required to maximize a female’s reproductive success of the predatory mite Kampimodromus aberrans Oudemans were studied under laboratory conditions. Newly emerged adult females of the stock colony of K. aberrans were placed individually on a bean leaf disc, and maintained at 25°C and 16:8 LD. A young male remained with a female for limited periods or continuously. Mating was a requisite for oocyte maturation and oviposition. Females which mated three to four times during their life and females in continuous presence of males, laid significantly and considerably more eggs than single-mated females. Virgin females lived the longest, and those in continuous presence of males the shortest. In all cases and irrespective of the number of matings, the sex ratio of the offspring was male-biased in the first three to four days of oviposition period, and female-biased in later days.     

Reproductive limits and heterogeneity of male twospotted spider mites

This paper determines reproductive limits and variation in performance of male twospotted spider mites Tetranychus urticae Koch when virgin females are provided ad libitum over the first eight days of adult life. Theree phases of male reproduction were studied: copulations, insemination and reproduction. An average one day old male copulated 15 times, inseminated 15 females, and contributed to 336 daughters. All parameters declined with age. The average male inseminated 70 females and contributed to 1145 daughters in the first days. Variability between males was small for all parameters considered. These data suggest that the number of sperm transferred at each insemination, rather than the number of inseminations, is the limiting step to higher male reproductive output.

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Résumé La reproduction est un processus qui nécessite généralement un mâle et une femelle. Cependant la biologie des populations ne s'est traditionnellement intéressée qu'à la contribution des femelles dans ce processus. Un effet de cet accent sur les femelles est que l'activité reproductrice des mâles a été très ignorée. Cet article examine, dans un contexte démographique, l'activité reproductrice des mâles de T. urticae, acarien arrhénotoque et phytophage. Trois séquences de l'activité reproductrice des mâles ont été examinées: 1) la copulation, 2) l'insémination, 3) la reproduction.En moyenne un mâle de 1 jour a copulé 15 fois, inséminé 15 femelles et a eu 336 filles. Pendant les 8 premiers jours, le mâle moyen a inséminé 70 femelles et a eu 1145 filles. Ces résultats suggèrent que le nombre de spermatozoïdes transférés à chaque insémination, plus que le nombre d'inséminations, est le facteur limitant d'une forte contribution du mâle à la reproduction.

     

Effects of multiple matings on reproductive fitness of male and female Diaeretiella rapae

Mating frequency and the amount of sperm transferred during mating have important consequences on progeny sex ratio and fitness of haplodiploid insects. Production of female offspring may be limited by the availability of sperm for fertilizing eggs. This study examined multiple mating and its effect on fitness of the cabbage aphid parasitoid Diaeretiella rapae McIntosh (Hymenoptera: Aphidiidae). Female D. rapae mated once, whereas males mated with on average more than three females in a single day. The minimum time lag between two consecutive matings by a male was 3 min, and the maximum number of matings a male achieved in a day was eight. Sperm depletion occurred as a consequence of multiple mating in D. rapae. The number of daughters produced by females that mated with multiple‐mated males was negatively correlated with the number of matings achieved by these males. Similarly, the proportion of female progeny decreased in females that mated with males that had already mated three times. Although the proportion of female progeny resulting from multiple mating decreased, the decrease was quicker when the mating occurred on the same day than when the matings occurred once per day over several days. Mating success of males initially increased after the first mating, but then males became ‘exhausted’ in later matings; their mating success decreased with the number of prior matings. The fertility of females was affected by mating with multiple‐mated males. The study suggests that male mating history affects the fitness of male and female D. rapae.     

POLYANDRY INCREASES OFFSPRING FECUNDITY IN THE BULB MITE

Abstract The common occurrence of polyandry continues to puzzle evolutionary biologists, as female reproductive success is thought to be limited mostly by her fecundity. Here we test whether females of the bulb mite, a species in which the females are highly promiscuous, benefit from polyandry in terms of increased fitness of their progeny. Females were given opportunity to mate with either one or six males, but the experiment was designed to allow the same number of matings per female in both groups, that is, irrespective of the number of males. We found that daughters of females mated to six males had significantly higher fecundity than daughters of females mated to one male, whereas other fitness components of progeny (male virility and longevity of both sexes) were not affected. These findings appear to support hypotheses proposing that multi-male mating enables females to exercise postcopulatory mate-choice (direct or indirect, via sperm competition) and thus accrue genetic benefits.     

Absence of Mate Choice and Postcopulatory Benefits in a Species with Extreme Sexual Size Dimorphism

Most hypotheses related to the evolution of female‐biased extreme sexual size dimorphism (SSD) attribute the differences in the size of each sex to selection for reproduction, either through selection for increased female fecundity or selection for male increased mobility and faster development. Very few studies, however, have tested for direct fitness benefits associated with the latter – small male size. Mecaphesa celer is a crab spider with extreme SSD, whose males are less than half the size of females and often weigh 10 times less. Here, we test the hypotheses that larger size in females and smaller size in males are sexually selected through differential pre‐ and postcopulatory reproductive benefits. To do so, we tested the following predictions: matings between small males and large females are more likely to occur due to mate choice; females mated to small males are less likely to accept second copulation attempts; and matings between small males and large females will result in larger clutches of longer‐lived offspring. Following staged mating trials in the laboratory, we found no support for any of our predictions, suggesting that SSD in M. celer may not be driven by pre‐ or post‐reproductive fitness benefits to small males.     

Wolbachia在山楂双叶螨中的感染及对寄主生殖的影响

【目的】共生菌Wolbachia在多种叶螨寄主中引起细胞质不亲和及适合度改变,影响寄主的生物学特性。山楂双叶螨Amphitetranychus viennensis是重要的果树害螨,常暴发成灾。本研究旨在明确Wolbachia在山楂双叶螨中的感染情况及对寄主生殖的影响。【方法】采集自然种群的山楂双叶螨,运用多位点序列分型技术（multilocus sequence typing, MLST）对其体内Wolbachia感染率及株系进行分析;通过杂交试验及生物学观察,分析感染Wolbachia对山楂双叶螨单雌产卵量、后代孵化率、性比及死亡率的影响。【结果】山楂双叶螨自然种群感染一种株系的Wolbachia （wVie）,该Wolbachia株系与小黑花椿象Orius strigicollis和丽蝇蛹集金小蜂Nasonia vitripennis中的Wolbachia株系亲缘关系较近,而与叶螨属Tetranychus叶螨感染的Wolbachia株系亲缘关系较远。Wolbachia与4种分化较小的线粒体单倍型相关联。Wolbachia感染雌虫与不感染雌虫产卵量没有显著差异（P>0.05）。不感染雌虫与感染雄虫交配,卵孵化率显著低于其他杂交组合 (P<0.05),但孵化率仍达近75%。各交配组合的后代性比及死亡率变化不明显（P>0.05）。【结论】Wolbachia在山楂双叶螨种群中的侵染历史较短,对山楂双叶螨的产卵力、后代性比、死亡率没有影响。Wolbachia在山楂双叶螨中诱导产生弱的CI表型。     

Occurrence of protandry and a female-biased sex-ratio in a sponge-associated water mite (Acari: Unionicolidae)

The sex ratio of aUnionicola crassipes-type mite from a pond in Alberta, Canada, was found to be significantly female-biased at the time of adult emergence. Male mites emerged earlier, but were later surpassed in number by the females. This protandry seems more likely to be due to the smaller size of the males and hence their faster developmental rate than to any mating advatage the male mites gain by early emergence. It is possible that group selection acting on the productivity of mite colonies with different proportions of low-sex-ratio producers has selected for female-bias. Water mites are not known to exhibit any atypical modes of reproduction (e.g.arrhenotoky), nor is it known whether pre-adult maleU. crassipes have a greater mortality rate than females, so the mechanism behind the skewed ratio is not known.     

The effect of interspecific mating on sex ratios in the twospotted spider mite and the Banks grass mite (Acarina: Tetranychidae)

Mixed populations of the twospotted spider mite (TSM),Tetranychus urticae (Koch), and the Banks grass mite (BGM),Oligonychus pratensis (Banks), occur on corn and sorghum plants in late summer in the Great Plains. Interspecific matings between these arrhenotokous species occur readily in the laboratory but yield no female offspring. The effect of interspecific mating on female: male sex ratios was measured by examining the F₁ progeny of females that mated with both heterospecific and conspecific males in no-choice situations. TSM females that mated first with BGM males and then with TSM males produced a smaller percentage of female offspring than TSM females that mated only with TSM males (43.1±5.8 and 78.9±2.8% females, respectively). Similarly, BGM females mated with heterospecific males and then with conspecific males produced fewer female offspring than females mated only with BGM males (55.7±5.2 and 77.5±2.5%, respectively). Lower female: male sex ratios were produced also by BGM females that mated with TSM males after first mating with conspecifics (62.4±3.4%). In mixed populations containing males of both species, females also produced lower female: male sex ratios, but these ratios were not as low as expected based on mating propensities and progeny sex ratios observed in no-choice tests. These data suggest that interspecific mating may substantially reduce female fitness in both mite species by reducing the output of female offspring, but in mixed populations this effect is mitigated by unidentified behavioral mechanisms.     

Sex dimorphism of life-history traits and their response to environmental factors in spider mites

Sex dimorphism is ubiquitous in the animal kingdom and can be influenced by environmental factors. However, relatively little is known about how the degree and direction of sex difference vary with environmental factors, including food quality and temperature. With the spider mites from the family Tetranychidae as subjects, the sex difference of life-history traits in responses to host plant and temperature were determined in this meta-analytic review. Across the 42 studies on 26 spider mite species (N?=?8057 and 3922 for female and male mites, respectively), female spider mites showed longer developmental duration than the males in all except two species. The direction of sex difference in development was consistent regardless of temperature and host plant. The 16 spider mite species in 33 studies generally showed female-biased longevity, with an overall effect size of 0.6043 [95%CI = 0.4054–0.8031]. Host plant significantly influenced the sex difference in longevity, where the males lived longer than females below 22.5 ℃, but the reverse was true at higher and fluctuating temperature. Host plant also influenced the magnitude of sex difference in longevity, with females living longer than males when reared on herbs but not on trees. This study indicated that life-history traits are highly variable between sexes under temperature and host plant influence, highlighting that environmental conditions can significantly shape the direction and magnitude of sexual dimorphism of life-history traits.

     

Sex-ratio adjustment in response to local mate competition is achieved through an alteration of egg size in a haplodiploid spider mite

Sex-ratio adjustments are commonly observed in haplodiploid species. However, the underlying proximate mechanisms remain elusive. We investigated these mechanisms in Tetranychus urticae, a haplodiploid spider mite known to adjust sex ratio in response to the level of local mate competition (LMC). In this species, egg size determines fertilization probability, with larger eggs being more likely to be fertilized, and thus become female. We explored the hypothesis that sex-ratio adjustment is achieved through adjustment of egg size. By using spider mites from a large population, we found that females produced not only a higher proportion of daughters under high levels of LMC, but also larger eggs. Moreover, in populations experimentally evolving under varying levels of LMC, both the proportion of females and the egg size increased with LMC intensity. These results suggest that sex-ratio adjustment in spider mites is mediated by egg size, although the causal relationship remains to be tested.     

Spermatozoa production in male <Emphasis Type="Italic">Varroa destructor</Emphasis> and its impact on reproduction in worker brood of <Emphasis Type="Italic">Apis mellifera</Emphasis>

Reproduction in Varroa destructor exclusively takes place within the sealed honey bee brood cell and is, therefore, limited by the duration of the postcapping period. Oogenesis, ontogenetic development and mating must be optimized to ensure the production of as many mated daughter mites as possible. One adult male mite has to mate with up to five sister mites and transfer 30–40 spermatozoa to each female. We analyzed the production and transfer of male spermatozoa during a reproductive cycle by counting all spermatozoa in the genital tracts of the male and daughter mites in 80 worker brood cells at defined times after cell capping. We could show that spermatozoa production in male mites is an ongoing process throughout their adult lifetime starting after the adult molt. The spermatozoa are transferred to the females in an early non-capacitated stage and require further maturation within the female’s genital tract. Our study points out that a Varroa male has at any time in the brood cell enough spermatozoa to inseminate all daughter mites but does not waste energy in producing a big surplus. In total one male produced, on average, 125 spermatozoa during a reproductive cycle in worker brood which is sufficient for successful matings with at least three daughter mites. Spermiogenesis in Varroa males represents therefore a further adaptation to the limited time available for reproduction.