Sexual reproduction of Daphnia pulex in a temporary habitat

Species of Daphnia (Crustacea: Cladocera) typically reproduce by cyclical parthenogenesis, in which a period of all-female parthenogenetic reproduction is followed by sexual reproduction. Sex in Daphnia is determined by the environment, with factors such as temperature, photoperiod and crowding stimulating the production of males and sexual females. Previous studies on Daphnia pulex from temporary pond habitats demonstrated the coexistence of male-producing and non-male-producing (NMP) females, as determined under crowding in the laboratory. A strong genetic component to this sex allocation variation suggested that sex expression in D. pulex is better described as a result of genotype-environment interaction. The present study examined the switch from parthenogenetic to sexual reproduction in two temporary-pond populations of D. pulex. Both populations showed a very early investment in sexual reproduction, independent of population density, by producing males very soon after the populations were reestablished from resting eggs in the early spring. Approximately 40% of the initial broods were male. Additional evidence for gender specialization was obtained by observing the sex of two or three successive broods for 85 individual females. Fifty-eight females produced successive broods of females, 13 females produced successive broods of males and 14 females produced successive broods which included both male and female broods. Females that produced successive female broods under natural conditions included a higher frequency of NMP females compared to a random sample of females, confirming the existence of NMP females. Sexual females were observed in both populations after the first appearence of males, suggesting that the presence of males may stimulate the production of sexual females. For D. pulex populations in a temporary environment, there appears to be an increased emphasis on sexual reproduction and a decreased influence of the environment on sex determination, compared to Daphnia populations in more permanent habitats. Received: 19 February 1996 / Accepted: 20 January 1997     

Clonal diversity and turnover in an overwintering Daphnia pulex population,and the effect of fish predation

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Food quality triggers the reproductive mode in the cyclical parthenogen <Emphasis Type="Italic">Daphnia</Emphasis> (Cladocera)

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Summary

The relationship between environmental factors, sex ratio, mode of reproduction, and female reproductive effort was examined in the cyclically parthenogenetic Daphnia magna. Female reproductive effort was found to decline before a significant production of males and sexual eggs takes place. Unlike factors such as crowding, poor nourishment, low (sometimes high) temperature and short or long day length, lowered reproductive effort is not a cue but rather an indicator of the selective advantage that would accrue from a changed sex ratio and mode of reproduction. The mechanism of the complex system of environmental sex determination in Daphnia is reviewed, and the adaptivity of ESD is discussed.     

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Dormancy is a common adaptation in invertebrates to survive harsh conditions. Triggered by environmental cues, populations produce resting eggs that allow them to survive temporally unsuitable conditions. Daphnia magna is a crustacean that reproduces by cyclical parthenogenesis, alternating between the production of asexual offspring and the sexual reproduction of diapausing eggs (ephippia). Prior to ephippia production, males (necessary to ensure ephippia fertilization) are produced parthenogenetically. Both the production of ephippia and the parthenogenetic production of males are induced by environmental factors. Here, we test the hypothesis that the induction of D. magna resting egg production shows a signature of local adaptation. We postulated that Daphnia from permanent ponds would produce fewer ephippia and males than Daphnia from intermittent ponds and that the frequency and season of habitat deterioration would correlate with the timing and amount of male and ephippia production. To test this, we quantified the production of males and ephippia in clonal D. magna populations in several different controlled environments. We found that the production of both ephippia and males varies strongly among populations in a way that suggests local adaptation. By performing quantitative trait locus mapping with parent clones from contrasting pond environments, we identified nonoverlapping genomic regions associated with male and ephippia production. As the traits are influenced by two different genomic regions, and both are necessary for successful resting egg production, we suggest that the genes for their induction co‐evolve.     

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Identification and expression analysis of a doublesex1 gene in Daphnia pulex during different reproductive stages

The gene doublesex (dsx) has shown deep conservation in the sex determination in many organisms. Environmental stimuli initiate a switch in the reproductive strategy of Daphnia pulex from asexual to sexual reproduction; however, occasionally, changes in environmental conditions will not lead to this transition. So study genetic responses to environmental stimuli and the molecular basis for the switch of reproductive stages are urgently needed. Therefore, we isolated and sequenced a D. pulex doublesex1 gene (Dpdsx1) and analyzed its expression and location by quantitative polymerase chain reaction (qPCR) and whole-mount in situ hybridization in D. pulex during different stages of reproduction. The predicted amino acid sequence has 335 amino acids that contained one DM domain and one dimerization domain, which is characteristic of insect orthologs of Dsx. Real-time PCR showed that Dpdsx1 expression decreased significantly (P?<?0.05) in different reproductive stages in the following order: male, parthenogenetic female, ephippial female, resting egg, and juvenile female. Whole-mount in situ hybridization revealed that Dpdsx1 is expressed in the first antennae, first thoracic limb and compound eye in males, whereas expression levels in the corresponding sites of parthenogenetic and ephippial females were relatively weak. Dpdsx1 could not be detected in the gonads of males or ephippial and parthenogenetic females. Taken together, these different reproductive stages’ and sex specific expression patterns are regulated temporally and spatially. We speculate that Dpdsx1 may involve in switching different stages of reproduction and in sexual differentiation in D. pulex.     

Chaoborus predation and delayed reproduction in Daphnia: a demographic modeling approach

I develop a demographic model that examines the impact of Chaoborus predation on the population dynamics and life history of Daphnia. Predation effects are determined through analysis of the various components of the predator-prey interaction (encounter, attack, strike efficiency), and are integrated into a stage-classified matrix population model. The model is parameterized with data from interactions between D. pulex and fourth-instar C. americanus. I test this model with two laboratory experiments that examine population growth of D. pulex under the influence of five different levels of Chaoborus predation. With the exception of a single predation treatment in each experiment, the model accurately predicted the observed reduction in Daphnia numbers with increasing Chaoborus predation. I then use this model to investigate the evolution of delayed reproduction in D. pulex that are exposed to Chaoborus. I ask whether delayed reproduction may evolve in Daphnia that are subjected to Chaoborus predation as a trade-off for the benefits of larger body size. The model predicts that the effectiveness of such a life history trade-off depends on the relative sizes of predator and prey. In some interactions between Chaoborus and Daphnia, increasing Daphnia body length by as little as 5% from base growth trajectories sufficiently increases fitness (by reducing vulnerability to Chaoborus predation) to compensate for the cost of delayed reproduction. In other interactions, however, increased body length provides no benefit to Daphnia (and may even reduce fitness), and selection would act against the evolution of delayed reproduction. This revised version was published online in July 2006 with corrections to the Cover Date.     

The impact of food quantity on UV-B tolerance and recovery from UV-B damage in Daphnia pulex

UV-B (290 nm) tolerance of Daphnia pulex, conditioned to four different food levels (Chlorophyta), was tested under standardized conditions with an artificial radiation source. Parameters measured were survival, percentage of egg bearing Daphnia and the number of juveniles produced after irradiation. UV-B tolerance of Daphnia pulex was found to be significantly improved with increasing food concentrations at all three parameters. The impact of the four different food concentrations on the photoreactivation system was tested with simultanous UV-B and white-light irradiation of Daphnia. Survival rate improved significantly with increasing food levels compared to solely UV-B irradiation. Photoreactivation had no effect on the reproductive parameters.     

THE ORIGIN AND GENETIC BASIS OF OBLIGATE PARTHENOGENESIS IN DAPHNIA PULEX

Sex in Daphnia is environmentally determined, and some obligately parthenogenetic clones of D. pulex have retained the ability to produce males. In the present study, males from 13 such clones were crossed to sexual females from closely related cyclical parthenogens both to determine whether the males were capable of producing viable hybrids and to determine the mode of reproduction of the hybrids. A total of 178 genetically confirmed hybrids were produced, with each of the 19 attempted crosses resulting in some viable hybrids. On average, only 34% of the hybrid eggs that initiated development survived to the reproductive stage, suggesting some incompatibility between the parents. The absence of any association between survivorship and parental or hybrid genotype indicated, however, that there is no specific genetic incompatibility associated with the marker loci used. The inability of most hybrids to produce normal resting eggs is further evidence of a general genomic incompatibility between the parents. Ten of the hybrids produced viable resting eggs, permitting tests to determine their mode of reproduction. Six of the 10 hybrids reproduced by cyclical parthenogenesis, like their maternal parent. The remaining four hybrids reproduced by obligate parthenogenesis, like their paternal parent, demonstrating that the genes suppressing meiosis can be transmitted by the male parent. These results support a model for the generation of new clones that involves the spread of genes suppressing meiosis and provide evidence that the high genotypic diversity observed in obligately parthenogenetic populations of D. pulex is a result of the multiple origin of new clones from the cyclical parthenogens. Evidence was also obtained suggesting that the obligately parthenogenetic clones carry a load of recessive deleterious genes.     

Does local adaptation to resources explain genetic differentiation among Daphnia populations?

Substantial genetic differentiation is frequently observed among populations of cyclically parthenogenetic zooplankton despite their high dispersal capabilities and potential for gene flow. Local adaptation has been invoked to explain population genetic differentiation despite high dispersal, but several neutral models that account for basic life history features also predict high genetic differentiation. Here, we study genetic differentiation among four populations of Daphnia pulex in east central Illinois. As with other studies of Daphnia, we demonstrate substantial population genetic differentiation despite close geographic proximity (<50 km; mean θ = 0.22). However, we explicitly tested and failed to find evidence for, the hypothesis that local adaptation to food resources occurs in these populations. Recognizing that local adaptation can occur in traits unrelated to resources, we estimated contemporary migration rates (m) and tested for admixture to evaluate the hypothesis that observed genetic differentiation is consistent with local adaptation to other untested ecological factors. Using Bayesian assignment methods, we detected migrants in three of the four study populations including substantial evidence for successful reproduction by immigrants in one pond, allowing us to reject the hypothesis that local adaptation limits gene flow for at least this population. Thus, we suggest that local adaptation does not explain genetic differentiation among these Daphnia populations and that other factors related to extinction/colonization dynamics, a long approach to equilibrium F_ST or substantial genetic drift due to a low number of individuals hatching from the egg bank each season may explain genetic differentiation.     

The influence of predator regime on reproductive traits in <Emphasis Type="Italic">Gammarus</Emphasis> <Emphasis Type="Italic">pulex</Emphasis> populations

Selection on traits conferring reduced predation may be opposed by selection on other traits associated with reproduction. Here, we examined the hypothesis that traits associated with reproduction in Gammarus pulex are driven by predation. We studied G. pulex originating from ponds with two different kinds of predator regimes: (1) ponds with fish—often large, non-gap-limited predators and (2) ponds without fish where invertebrates are the dominant predators—often small, gap-limited predators with a much more restricted prey size range. We examined the body size of males and females in G. pulex amplexus pairs originating from fish and fishless ponds. We also examined, in the laboratory, their mating success, the number of offspring per female and offspring mortality under different rearing conditions, with or without fish cue. Mating success, defined as the percentage of amplexus pairs that produced live offspring, was higher for G. pulex from fishless ponds independent of rearing condition. Individuals from fish ponds were larger and they produced a higher number of offspring which tended to be related to female body size. Offspring mortality was higher in populations from fish ponds compared to populations from fishless ponds. Despite the higher offspring mortality, females from fish ponds had a higher number of offspring alive after 13 weeks, which is the approximate time it takes for G. pulex to reach maturity. Our data imply that no trade-off between reducing body size to reduce mortality caused by fish and maximising reproductive success exist in G. pulex from fish ponds. The strategy with many offspring may be the correct strategy in fishponds where predation pressure generally is higher than in fishless ponds.