Effect of food concentration on the production and viability of resting eggs of the rotifer Brachionus: implications for the timing of sexual reproduction

1. Life‐table experiments with Brachionus calyciflorus test several hypotheses related to the idea that sexual reproduction in monogonont rotifers should occur when food resources are favourable. 2. The food concentration necessary for a fertilised mictic female to produce one phenotypically normal resting egg was higher than that for an amictic female to produce one daughter. At the lowest concentration of Cryptomonas erosa (1.25 × 10³ cells mL^?1), the lifetime fecundity of these two types of females was 0.9 and 1.4, respectively. 3. The lifetime fecundity of both fertilised mictic females and amictic females increased with food concentration to 3.4 resting eggs and 15.2 daughters female^?1, respectively. The approach to maximal fecundity with increasing food concentration was more rapid for fertilised mictic females, such that their lifetime fecundity relative to that of amictic females gradually decreased from 0.64 (at 1.25 × 10³ C. erosa mL^?1) to 0.22 (at 2.5 × 10⁴ C. erosa mL^?1). 4. The probability of a fertilised mictic female producing one or more abnormal resting eggs during her lifetime was high (approximately 75%). The mean proportion of abnormal eggs produced per female varied among the different food‐concentration treatments (26–38%) but was not higher at the low food concentrations. 5. The proportion of normal resting eggs that hatched was high (51–71%); those produced at low food concentrations were no less likely to hatch than those produced at high food concentrations. No abnormal resting eggs hatched. 6. The probability of a fertilised mictic female producing an abnormal resting egg increased rapidly with her age at all food concentrations. The probability of a normal resting egg hatching declined with maternal age at the low food concentration in one of two experiments. 7. The results support the idea that induction of mictic females should occur when food resources are good. Coincidence of sexual reproduction with low food availability risks low production of resting eggs for several reasons. Population size may be small, with a low probability of encounters between young mictic females and males, and fertilised mictic females may be unable to mature and produce resting eggs.     

Optimal rates of bisexual reproduction in cyclical parthenogens with density-dependent growth

This work explores theoretical patterns of reproduction that maximize the production of resting eggs and the long-term fitness of genotypes in cyclical parthenogens. Our focus is on density-dependent reproduction as it influences the consequences of a trade-off between producing amictic daughters – which reproduce parthenogenetically and subitaneously – and producing mictic daughters – which undergo meiosis and bisexual reproduction. Amictic females increase competitive ability and allow the population to achieve a larger size; mictic females directly contribute to population survival through harsh periods by producing resting eggs. Although morphologically indistinguishable, the two types of females differ greatly in their ecological and reproductive roles. What factors underlie the differential allocation of resources to produce amictic and mictic females? Using a demographic model based on readily accessible parameters we demonstrate the existence of a frequency of mictic females that will maximize the population's long-term fitness. This frequency, termed the optimal mictic ratio, m_o, is 1 ? (q/b)^1/2, where q is the mortality rate and b is the maximum birth rate. Using computer simulation we compared the fitness of a population with this constant mictic ratio with populations having multiple switches from complete parthenogenetic growth to complete allocation in mixis (mictic ratio either 0 or 1). Two important conclusions for optimal mixis in density-dependent growth conditions are: (1) intermediate mictic ratios are optimal, and (2) optimal mictic ratios are higher when habitat conditions are better. Physiological cues responding to differences in birth and death rates are common so that it is possible that populations may adjust their relative rates of mictic and amictic female production in response to environmentally induced changes to the optimum mictic ratio. Our analysis demonstrates that different patterns of mixis are expected in different type of habitats. Since the optimal mictic ratio is sensitive to the effects of a variety of environmental challenges, our model makes possible a new means to evaluate life history evolution in cyclical parthenogens.     

Endogenous regulation of environmentally induced sexuality in a rotifer: a multigenerational parental effect induced by fertilisation

SUMMARY 1. Sexual reproduction in the heterogonic life cycle of many rotifers occurs when amictic females, which produce diploid eggs developing parthenogenetically into females, are environmentally induced to produce mictic females. Mictic females produce haploid eggs which develop parthenogenetically into males or, if fertilised, into resting eggs – encysted embryos which develop into amictic females after an obligatory diapause. 2. A Florida strain of Brachionus calyciflorus was used to test the prediction that amictic females hatching from resting eggs (Generation 1), and those from the next few parthenogenetic generations, have a lower propensity to produce mictic daughters in response to crowding than those from later parthenogenetic generations. In 10 replicate clones, populations initiated by amictic females from generations 1, 5, 8, 12 and 18 were exposed to a standardised crowding stimulus, and the proportion of mictic females in the populations was determined. These proportions varied significantly across generations and clones. They were very low in the early generations and gradually increased to a mean of about 0.5 at Generation 12. 3. The mechanism for the transgenerational plasticity in response to crowding is not known. One possibility is that resting eggs contain an agent from their fertilised mictic mother's yolk gland that prevents development into mictic females and is transmitted in increasingly low concentrations through successive parthenogenetic generations of amictic females. 4. This parental effect may contribute to clonal fitness by ensuring that a clone developing from a resting egg will attain a higher population size through female parthenogenesis before maximising its commitment to sexual reproduction, even in the presence of a crowding stimulus from a high population density of other clones. Therefore, the number of resting eggs to which a clone contributes its genes should be maximised. 5. The clonal variation in propensity to produce mictic females in this strain indicates genetic variation in the trade‐off between maximising population growth via female parthenogenesis and increasing the probability of producing at least some resting eggs before local extinction from the plankton.     

Effect of diazinon on life stages and resting egg hatchability of rotifer Brachionus plicatilis

The effects of organophosphate pesticide, diazinon, on life history parameters and hatchability of resting eggs of rotifer Brachionus plicalitis were assessed. Newly hatched (<1 h-old) neonates were individually cultured in six varying concentrations (0/control, 0.1, 1.0, 2.5, 5.0 and 10.0 mg/l) of diazinon. The life history parameters such as time (h) the rotifers bear first egg and release first neonate, reproductive period, net reproductive rate, mixis, intrinsic rate of population increase, and life span were evaluated. Results showed that among the life history parameters, the time the rotifers took to release neonates is the most sensitive, giving the lowest EC₅₀ value of 1.24 mg/l. The fecundity of maternal females, amictic and mictic daughters was also investigated. Rotifers exposed to 10.0 mg/l produced significantly fewer amictic daughters, and at this concentration, rotifers did not produce any mictic daughter. At 5.0 mg/l, the number of male offspring was significantly lower than the control. Furthermore, the hatchability of resting eggs produced by the rotifers was evaluated when exposed to diazinon: from birth until they produced resting eggs (early development); during late developmental stage of resting eggs (before diapause); and during diapausing stage. The hatchability of the resting eggs was not affected when exposure was timed at late developmental and diapausing stages. Overall results showed that even though amictic females reproduced normally in the presence of low-concentration of diazinon, sexual reproduction is severely affected, especially the hatchability of resting eggs when the exposure was timed on its early developmental stages. Guest editors: S. S. S. Sarma, R. D. Gulati, R. L. Wallace, S. Nandini, H. J. Dumont & R. Rico-Martínez Advances in Rotifer Research     

Induction of mictic females in the rotifer Brachionus: oocytes of amictic females respond individually to population-density signal only during oogenesis shortly before oviposition

1. One at a time during the reproductive period of amictic females, oocytes fill with yolk and undergo a mitotic maturation division (oogenesis), are oviposited as single cells, and then develop parthenogenetically into females. Sexual reproduction in Brachionus and several other genera is initiated when amictic females are crowded and oviposit some eggs induced to differentiate into mictic females. Mictic females produce haploid eggs that can develop parthenogentically into males or be fertilised and develop into diapausing embryos called resting eggs. 2. This study examines the time when oocytes in amictic females respond to maternal population density. Is the fate of all oocytes in the germarium irreversibly determined during the early postnatal life of the mother, or is each oocyte labile until just before oviposition? In the former case, the probability of an amictic female producing a mictic daughter at any time throughout her reproductive period would reflect the population density she experienced while young and not that at the time she oviposited an egg. 3. Amictic females of two clones of a Florida strain of B. calyciflorus were cultured singly from birth at a low or high density (in a large or small volume) until about halfway through their reproductive period and then switched (experimental treatment), or not (control treatment), to the other density condition. The results indicate that the female fate of an oocyte is determined by maternal population density during oogenesis. Eggs oviposited soon after transfer from low to high density had the same, or a higher, probability of becoming mictic females compared with those produced by control females kept at the high density; eggs oviposited after transfer from the high to the low density had the same low probability of becoming mictic females as those produced by control females kept at the low density. 4. Control females kept at the high density were less likely to produce mictic daughters as they aged. This decline is not because of a decreased propensity of older females to respond to crowding, as older females responded maximally when transferred from a low to a high population density. 5. As oocytes in amictic females respond to maternal population density only during oogenesis, there is a negligible lag between the population‐density signal in the environment and the commitment to sexual reproduction. This minimises the obligatory two‐generation lag between this signal and production of resting eggs, and thus reduces the possibility that crowding will lead to food limitation before production of these eggs.     

Life history characteristics of three types of females in Brachionus calyciflorus Pallas (Rotifera) fed different algae

This study describes the life history characteristics of amictic, unfertilized mictic and fertilized mictic females of the rotifer Brachionus calyciflorus cultured individually on two different algae at 0.1 mg ml^–1 food concentration and 27 °C. The duration of the juvenile period of amictic females was significantly shorter on Chlorella pyrenoidosa Chick than on Scenedesmus obliquus Kütz or both algae together. The duration of the juvenile period of unfertilized mictic females was significantly longer, and the number of eggs produced by amictic females was significantly larger on Chlorella pyrenoidosa than on S. obliquus. When fed the same type of alga, the duration of the juvenile period of the fertilized mictic females was the longest among the three types of females, and the durations of the reproductive period of the amictic females and the post-reproductive period of the fertilized mictic females were longer than, or equal to those of the other two types of females, respectively. The number of eggs produced by an unfertilized mictic female was the largest among the three types of females, and that of amictic females was larger than or equal to that of fertilized mictic females, depending on the type of diet.     

Isolation of mixis-related genes from the rotifer <Emphasis Type="Italic">Brachionus plicatilis</Emphasis> using subtractive hybridization

The monogonont rotifer Brachionus plicatilis produces resting eggs through sexual reproduction (mixis), which is affected by external and internal factors. We collected resting eggs from rotifers cultured at 15 and 25°C and hatched them with and without 14-day dormancy in the dark. Stem females hatched from both conditions were further cultured at 15, 20 and 25°C. We obtained two phenotypes, one with high mixis (more than 50%), which was hatched from resting eggs formed at 15°C without dormancy, and another in which sexual reproduction occurred at 25°C and resting eggs were formed at 15°C with a 14-day dormancy. In the latter phenotype, mictic females appeared at 15°C, but not at 25°C. Using subtractive hybridization, we isolated one gene from the latter phenotype of females that had no significant similarity to known genes in BLAST searches. We propose that this gene is unique to rotifer mictic reproduction. Ongoing characterization of this gene attempts understand its role in mixis.     

Influence of the age of algae fed to rotifers (Brachionus plicatilis O.F. Müller) on the expression of mixis in their progenies

Summary The sequence of the appearance of mixis in the rotifer Brachionus plicatilis was followed among the descendents of amictic rotifers transferred from a high salinity media (40 S) to a low one (9 S). All the neonates that hatched from the amictic eggs, after being transferred to a low salinity, were amictic. Each one of these neonates was cultured individually and its offspring removed periodically every 8–10 h. It was observed that throughout their reproductive phase, these parental females retained their potential to produce either mictic or amictic offspring. All the first produced neonates developed into amictic females, but among those produced later, three patterns were prevalent. The prevalent pattern (type A) was one in which the probability of a neonate being mictic increased towards the middle of the parents' reproductive phase and was followed by a slow decline. In the second pattern (type B), the probability of a daughter being mictic was constant throughout the parents' reproductive phase. It is suspected that the quality of food supplied to the rotifers determines the appearance of patterns, A, B or C. It is postulated that the innate capacity of rotifers to undergo mixis is genetically controlled, while its expression is modulated by environmental conditions.     

Incomplete induction of mixis in <Emphasis Type="Italic">Brachionus calyciflorus</Emphasis>: patterns of reproduction at the individual level

In the rotifer Brachionus calyciflorus mictic-female production is density-dependent and appears to be induced by a chemical—a quorum sensing molecule—produced by the females themselves. Even at the highest densities, however, populations never become entirely mictic: i.e., some amictic females continue to be produced. Surprisingly, the phenomenon also occurs in clonal laboratory populations with genetically identical individuals. Here, we study how this ecologically adaptive phenomenon is generated at the level of individual reproducing females. In a life-history experiment we subjected 123 amictic females of a clone of B. calyciflorus separately to a daily renewed stimulus of culture medium conditioned at a density of 30 females ml⁻¹. For each of these mothers we isolated the lifetime offspring individually and recorded whether these females were amictic or mictic. Mothers produced on average 16 offspring but none of the mothers produced 100% mictic offspring; the average proportion of mictic females was 30%, despite the extremely strong stimulus. The distribution of amictic vs. mictic offspring was not uniform over the mothers’ lifetime. Early and late offspring had a low probability of being mictic whereas mid-aged mothers produced the highest proportion of mictic daughters (up to 56%). We conclude that not all oocytes of B. calyciflorus can be turned into mictic females, even when the mictic-female-inducing stimulus is extremely high. Propensity to become a mictic female also depends on the rank of an egg within a female’s offspring production. Despite these regularities, we observed considerable stochastic variability with respect to individual mothers’ life histories. Guest editors: S. S. S. Sarma, R. D. Gulati, R. L. Wallace, S. Nandini, H. J. Dumont & R. Rico-Martínez. Advances in Rotifer Research.     

Maternal Effect by Stem Females in <Emphasis Type="Italic">Brachionus plicatilis</Emphasis>: Effect of Starvation on Mixis Induction in Offspring

We examined whether starvation during the initial period of life in stem females affected reproductive characteristics of the offspring. Starvation treatment had different effects on rotifers hatched from resting eggs and those hatched from amictic eggs. When stem females experienced starvation after hatching, this induced a higher percentage of mixis in their offspring. When the same starvation treatment was applied to rotifers hatched from amictic eggs, there was no effect on the induction of mixis. It is probable that stem females hatched from resting eggs have specific features that are vulnerable to unfavorable environmental conditions, and that these features can be inherited by their offspring through the maternal cytoplasm.     

Control of sexuality in Asplanchna brightwelli: threshold levels of dietary tocopherol and modification of tocopherol response by exogenous and endogenous factors

Ingestion of one prey rotifer containing about 0.02 pg tocopherol was sufficient to cause young amictic females to produce a high proportion of mictic daughters. Varying the concentration of emulsified tocopherol ol and the population density of amictic females suggested that mictic-female induction approached an all-or-nothing response at relatively high population densities and increased with population density only when population densities were very low. Amictic females hatching from resting eggs were less likely to produce mictic daughters than those hatching from parthenogenetic eggs.     

Delayed mixis in rotifers: an adaptive response to the effects of density-dependent sex on population growth

In most cyclically parthenogenetic life cycles, sex is neededto produce resting stages. In several species of cyclicallyparthenogenetic rotifers, some generations of clones are notresponsive to a density-dependent signal that triggers sexualfemale production. These unresponsive rotifers hatch from restingeggs and typically pass 8–12 generations of female parthenogenesisbefore becoming receptive to the mixis signal. We addressedthe selection for mixis delay using a simulation model. A delayof sexual reproduction could increase population growth throughparthenogenesis and thus the number of resting eggs ultimatelyproduced. In a monomorphic population without mixis delay, wedetermined the optimal ratio of mictic to amictic females (mixisratio) to be 45%, and the optimal population density thresholdfor induction of mictic females (mixis threshold) to be 82 rotifersL^–1. This mixis pattern, however, was not an evolutionarilystable strategy. A mixis ratio of 14% and threshold of 70 rotifersL^–1 proved to be resistant to invasion by other mixispatterns. When we gave this phenotype a mixis delay of 8–10days, it could invade a population with the same mixis pattern,but lacking a mixis delay. The advantage of delaying mixis wasrelatively small, suggesting that a polymorphism is possible.     

Effect of incubation and preservation on resting egg hatching and mixis in the derived clones of the rotifer Brachionus plicatilis

The marine rotifer Brachionus plicatilis typicus (Clone 8105A, Univ. of Tokyo) was cultured in 500 ml beakers to form resting eggs. Tetraselmis tetrathele was used as a culture food. Just after formation, resting eggs were exposed to various temperature (5–25 °C) and light regimes (24L: OD and OL : 24D). When eggs were exposed to light just after formation, the eggs hatched sporadically over a month. No hatching was observed for six months when eggs were preserved under dark conditions regardless of the temperature. These eggs hatched simultaneously after being exposed to light and eggs preserved at 5 °C showed twice as high hatching rate (40%) as that of eggs preserved at 15–25 °C (24%). Clones from resting eggs that were kept under different temperature and light regimes were reared individually to the third generation. Incubation at 25 °C with lighting produced the highest (5.4% and 5.2 %) rate of mictic females during their 2nd and 3rd generations, respectively. The lowest rates (0 and 1.5%) were found when the eggs were kept at 5 °C in total darkness for six months. A lower rate of amictic female production was found in clones with higher rates of mixis.     

Intraclonal variation in propensity for mixis in several rotifers: variation among females and with maternal age

In 14 previously published experiments with clones of three species of Brachionus, Epiphanes ukera, and Rhinoglena frontalis, females cultured singly in small volumes from birth through most of their reproductive period usually produced some mictic daughters. Here, these data are analyzed to test two hypotheses: the propensity of females in a clone to produce mictic daughters will vary significantly among females, and will decrease with female age. Significant heterogeneity (χ²) among replicate females was demonstrated in two clones of B. calyciflorus from Florida, in single clones of this species from Georgia, Texas, Spain, and Australia, in a clone of B. angularis from Argentina, and in single clones of E. ukera and R. frontalis from Germany. No significant heterogeneity was found in two other clones of B. calyciflorus from Florida and in a clone of B. variabilis from Spain. Significant heterogeneity among females of a clone could be caused by chance fluctuations during development, differences in birth order, or epimutations. This heterogeneity is an important component of a bet-hedging strategy to balance production of diapausing fertilized eggs and future population growth by female parthenogenesis. The propensity of a female to produce mictic daughters did not decrease with her age. In experiments with six different clones from four strains of B. calyciflorus, and with single clones of E. ukera and R. frontalis, only one clone of B. calyciflorus showed significant variation (ANOVA) in the proportion of mictic daughters produced in three or four successive one- or two-day periods. In this clone the proportion of mictic daughters increased with maternal age. Guest editors: S. S. S. Sarma, R. D. Gulati, R. L. Wallace, S. Nandini, H. J. Dumont & R. Rico-Martínez Advances in Rotifer research     

Polymorphism in stem females and successive parthenogenetic generations in Brachionus calyciflorus Pallas

We have described the polymorphism in the hatchlings of resting eggs and the morphological variations between the stem females hatched from resting eggs and their successive parthenogenetic generations in the rotifer Brachionus calyciflorus. We hatched resting eggs of B. calyciflorus in two different culture mediums: unconditioned medium (IOM) and Asplanchna-conditioned (ACM). The hatching rate of resting eggs in IOM and ACM were 32.5% and 28.5%, respectively, and showed no significant difference. Stem females hatching from these resting eggs had three morphotypes (unspined, single short-spined, and two short-spined) and over 80% of these females were spineless ones. Moreover, the frequency of each morphotype stem females showed similar tendency in IOM and ACM. The production of a variety of morphotypes among stem mothers—rather than all unspined as has been previously reported for this species—may be regarded as a form of bet-hedging in this population of B. calyciflorus. Phenotypic changes in morphology between the stem females hatched from resting eggs and their successive parthenogenetic generations in B. calyciflorus were found. The possible mechanisms, responsible for high proportion of spineless phenotype at early generations from resting eggs and increased spined phenotype in successive parthenogenetic generations, were discussed in the article.     

Effects of Juvenile Hormone and Precocene on the Reproduction of Brachionus calyciflorus

We studied the effects of juvenile hormone and precocene on reproduction of the rotifer Brachionus calyciflorus. Amictic females of B. calyciflorus that were 2‐4 hours old were exposed to different concentrations of juvenile hormone (0.004, 0.02, 0.1, 0.5, 2.5, 12.5 mg/L) and/or precocene (0.05, 0.25, 0.75, 3.75, 7.5 mg/L) for 24 h. They were then transferred to a new medium without hormone and checked every 2 h during the next 48 h, and thereafter monitored daily until the individual died. Precocene had no effects on the length of the rotifer juvenile period, hatching time of the first neonate, lifetime reproduction, or the mixis ratio. In contrast, juvenile hormone at 0.5, 2.5, and 12.5 mg/L significantly prolonged the juvenile period by 6.1, 9.2, and 8.6%, respectively. When 26‐28‐h‐old amictic females were exposed to the same concentration series of juvenile hormone or precocene, precocene at 3.75 mg/L resulted in an increase in lifetime reproduction of 30.39%. However, at 0.75 and 3.75 mg/L precocene, a significantly lower percentage of mictic females was found, whereas juvenile hormone had no effect on the lifetime reproduction or mixis ratio. The population growth test showed that juvenile hormone had significant effects on the population growth rate and mixis ratio, but no effect on resting egg production. In comparison, precocene had no effect on any of these parameters. (© 2012 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

孤雌生殖累积世代数和雌体年龄对萼花臂尾轮虫繁殖的影响

采用单个体培养方法,研究了孤雌生殖的累积世代数和雌体年龄对萼花臂尾轮虫混交雌体形成和产卵量的影响,结果表明,随着轮虫孤雌生殖累积世代数和增加,各代中的总混交雌体百分率呈减小的趋势,年轮的雌体可产生较多的混交雌体,非混交雌体所产后代中的总混交雌体百分率具有随其祖母年龄的增大而增大的趋势,孤雌生殖的累积世代数对轮对轮虫非混交雌体的平均产卵量无显著的影响,非混交雌体的年龄对其报代的平均产卵量亦无显著的影响。     

The Effect of Food Concentration on the Life History of Three Types of Brachionus calyciflorus Females

The effect of food concentration on the life history of three types of Brachionus calyciflorus females (amictic, unfertilized mictic and fertilized mictic female) was studied with replicated individual cultures at 25 ° and at four food concentrations (1.5, 3.0, 6.0 and 9.0 × 10⁶ cells mL^—1) of Scenedesmus obliquus. There were highly significant effects of both food concentration and female type, independently and in interaction on the duration of juvenile period of the rotifer, but neither were the effects on the duration of post‐reproductive period and mean life‐span. The duration of juvenile period of unfertilized mictic female at the food concentration of 9.0 × 10⁶ cells mL^—1 was the longest among all the food concentration‐female type combinations. Both food concentration and female type influenced significantly the duration of reproductive period and the number of eggs produced by each type of female per life cycle, respectively. There was, however, no significant interaction between food level and female type. Among the three types of females, the number of eggs produced by an unfertilized mictic female was the largest, and that of a fertilized mictic female was the smallest.     

Reduced investment in sex as a cost of inducible defence in Brachionus calyciflorus (Rotifera)

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Induction of sexual reproduction and resting egg production in Brachionus Plicatilis reared in sea water

Brachionus plicatilis raised in our laboratory in sea water reproduces asexually even under high crowding conditions (at least 40 individuals per ml). Amictic females were induced to produce mictic females, males and resting eggs by reducing the concentration of the sea water culture medium. Mictic females and males appeared predominantly among the progeny produced by the amictic females during 4 days following their transfer into 25% sea water. Resting eggs appeared first 5–12 days after the onset of the experiment. Following the disappearance of males, the culture consisted of amictic females.Resting eggs produced by the method described above may be preserved for at least three months at –14°C or by desiccation at room temperature. Under the appropriate experimental conditions, resting eggs hatch into amictic females. Since B. plicatilis is one of the most commonly used food sources of fish larvae in aquaculture, the methods reported here may offer an easy and versatile way of preserving rotifer culture stock to be used on demand.