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Onset of kairomone sensitivity and the development of inducible morphological defenses in Daphnia pulex

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Linda Carolin Weiss at Ruhr University Bochum
Linda Carolin Weiss
Esther Heilgenberg
Esther Heilgenberg
Esther Heilgenberg
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Lisa Deussen
Lisa Deussen
Lisa Deussen
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Sina M. Langer at Ruhr University Bochum
Sina M. Langer
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Abstract and Figures

The micro-crustacean Daphnia pulex is a model species for studying predator-induced defenses. When exposed to chemical cues released by its predator, the phantom midge larvae Chaoborus (Diptera), it develops protective neckteeth that reduce the predator’s success of predation in the juvenile instars. Defensive traits need to be expressed as soon as possible, which requires an early sensitivity to predator cues. We investigated the exact kairomone-sensitive period in three D. pulex strains and the timeline of neckteeth expression in early juvenile instars. We divided embryonic development into five major stages based on successive morphological landmarks. We exposed animals in these developmental stages to kairomones in order to determine the sensitive periods for neckteeth expression in the 1st and 2nd juvenile instar. Our results indicate that kairomone sensitivity starts during embryogenesis when compound eye spots begin to fuse and egg membranes are shed. Neckteeth develop with a stage-dependent time lag, being shorter when exposed in the first kairomone-sensitive stage and longer when exposed in the following developmental stages. Evolution of early kairomone sensitivity and fast defense development is a crucial step in D. pulex’s defenses against Chaoborus as it allows for protection of the most vulnerable juvenile stages.
Periods of kairomone treatment during development of D. pulex embryos. A Kairomonestimulated embryonic stages are indicated in gray. Stimulation covered multiple and individual developmental stages. D. pulex mothers holding eggs in their ovaries were transferred into 50-ml glass vials holding 40 ml water or the respective kairomone concentrations adjusted for clones R9, K2, and SBL. Data acquisition was performed in the 1st and 2nd juvenile instar. B Kairomone stimulation (gray) and control treatments during embryonic stage IV to precisely determine the onset of kairomone sensitivity in D. pulex clones R9 and SBL
Periods of kairomone treatment during development of D. pulex embryos. A Kairomonestimulated embryonic stages are indicated in gray. Stimulation covered multiple and individual developmental stages. D. pulex mothers holding eggs in their ovaries were transferred into 50-ml glass vials holding 40 ml water or the respective kairomone concentrations adjusted for clones R9, K2, and SBL. Data acquisition was performed in the 1st and 2nd juvenile instar. B Kairomone stimulation (gray) and control treatments during embryonic stage IV to precisely determine the onset of kairomone sensitivity in D. pulex clones R9 and SBL
… 
Neckteeth expression of D. pulex clone K2 at 20 larvae/ l. A All induction periods that cover the stage IV (I–V; II–V; III– V; IV–V) significantly induce neckteeth expression in the 1st juvenile instar (see Supplementary Table 1). B All induction periods that cover stage V (I–V; II–V; III–V; IV–V) significantly induce neckteeth expression in the 2nd juvenile instar, (see Supplementary Table 2)
Neckteeth expression of D. pulex clone K2 at 20 larvae/ l. A All induction periods that cover the stage IV (I–V; II–V; III– V; IV–V) significantly induce neckteeth expression in the 1st juvenile instar (see Supplementary Table 1). B All induction periods that cover stage V (I–V; II–V; III–V; IV–V) significantly induce neckteeth expression in the 2nd juvenile instar, (see Supplementary Table 2)
… 
Neckteeth expression of D. pulex clone R9 at 10 larvae/ l. A In the 1st juvenile instar, all induction periods that cover stage IV (I–V; II–V; III–V; IV–V) significantly induce neckteeth expression (see Supplementary Table 3). B In the 2nd juvenile instar, all induction periods that cover stage V (I– V; II–V; III–V; IV–V) significantly induce neckteeth expression (see Supplementary Table 4)
Neckteeth expression of D. pulex clone R9 at 10 larvae/ l. A In the 1st juvenile instar, all induction periods that cover stage IV (I–V; II–V; III–V; IV–V) significantly induce neckteeth expression (see Supplementary Table 3). B In the 2nd juvenile instar, all induction periods that cover stage V (I– V; II–V; III–V; IV–V) significantly induce neckteeth expression (see Supplementary Table 4)
… 
Neckteeth expression of D. pulex clone SBL at 40 larvae/l. A In the 1st juvenile instar, all induction periods that cover stage IV (I–V; II–V; III–V; IV–V) significantly induce neckteeth expression (see Supplementary S Table 5). B In the 2nd juvenile instar, all induction periods that cover stage V (I– V; II–V; III–V; IV–V) significantly induce neckteeth expression (see Supplementary Table 6)
Neckteeth expression of D. pulex clone SBL at 40 larvae/l. A In the 1st juvenile instar, all induction periods that cover stage IV (I–V; II–V; III–V; IV–V) significantly induce neckteeth expression (see Supplementary S Table 5). B In the 2nd juvenile instar, all induction periods that cover stage V (I– V; II–V; III–V; IV–V) significantly induce neckteeth expression (see Supplementary Table 6)
… 
Percentage of 1st instar D.pulex juveniles (clones SBL; K2; R9) with spontaneous neckteeth expression. Neckteeth occur in some clones even without Chaoborus kairomone induction. The number of tested juveniles per clone in total is shown above each bar (n)
+2
Percentage of 1st instar D.pulex juveniles (clones SBL; K2; R9) with spontaneous neckteeth expression. Neckteeth occur in some clones even without Chaoborus kairomone induction. The number of tested juveniles per clone in total is shown above each bar (n)
… 
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PRIMARY RESEARCH PAPER
Onset of kairomone sensitivity and the development
of inducible morphological defenses in Daphnia pulex
Linda C. Weiss .Esther Heilgenberg .Lisa Deussen .
Sina M. Becker .Sebastian Kruppert .Ralph Tollrian
Received: 14 December 2015 / Revised: 1 May 2016 / Accepted: 2 May 2016 / Published online: 9 May 2016
ÓSpringer International Publishing Switzerland 2016
Abstract The micro-crustacean Daphnia pulex is a
model species for studying predator-induced defenses.
When exposed to chemical cues released by its
predator, the phantom midge larvae Chaoborus
(Diptera), it develops protective neckteeth that reduce
the predator’s success of predation in the juvenile
instars. Defensive traits need to be expressed as soon
as possible, which requires an early sensitivity to
predator cues. We investigated the exact kairomone-
sensitive period in three D. pulex strains and the
timeline of neckteeth expression in early juvenile
instars. We divided embryonic development into five
major stages based on successive morphological
landmarks. We exposed animals in these develop-
mental stages to kairomones in order to determine the
sensitive periods for neckteeth expression in the 1st
and 2nd juvenile instar. Our results indicate that
kairomone sensitivity starts during embryogenesis
when compound eye spots begin to fuse and egg
membranes are shed. Neckteeth develop with a stage-
dependent time lag, being shorter when exposed in the
first kairomone-sensitive stage and longer when
exposed in the following developmental stages. Evo-
lution of early kairomone sensitivity and fast defense
development is a crucial step in D. pulex’s defenses
against Chaoborus as it allows for protection of the
most vulnerable juvenile stages.
Keywords Daphnia Kairomone-sensitive stages
Chaoborus Inducible defenses Time lags
Neckteeth
Introduction
The evolutionary ‘arms race’ between predators and
prey has generated various anti-predator adaptations.
These adaptations may even be inducible, so that they
develop only upon an increased predation risk.
Inducible defenses include morphological peculiari-
ties (e.g., thorns, spines, strengthened body armor),
behavioral changes (e.g., adaptive migration patterns),
and life-history shifts (e.g., somatic growth traded for
reproduction (DeWitt, 1998; Tollrian & Harvell,
1999)).
Four factors have emerged as relevant in the
evolution of inducible anti-predator phenotypes:
(i) heterogeneous predation risk, (ii) reliable cues
indicating a potential risk, (iii) the defense must be
Handling editor: Piet Spaak
Electronic supplementary material The online version of
this article (doi:10.1007/s10750-016-2809-4) contains supple-
mentary material, which is available to authorized users.
L. C. Weiss (&)E. Heilgenberg L. Deussen
S. M. Becker S. Kruppert R. Tollrian
Department of Animal Ecology, Evolution and
Biodiversity, Ruhr-University Bochum, Universita
¨tsstraße
150, 44801 Bochum, Germany
e-mail: linda.weiss@rub.de
123
Hydrobiologia (2016) 779:135–145
DOI 10.1007/s10750-016-2809-4
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... These studies have highlighted the importance of the neckteeth defence as a model for continuous phenotypic plasticity. They have shown that the strength and duration of induction varies according to the stage of development and depends on the concentration of predator cue (Beckerman et al., 2010;Naraki et al., 2013;Weiss et al., 2016). Evidence also suggests that there is a threshold for adaptive phenotypes to evolve, which is driven by the trade-off between the fitness costs and benefits of neckteeth production under different levels of predation risk (Hammill et al., 2008). ...
... The neckteeth defence is composed of a swollen area on the back of the head (neck-pedestal) and spikey projections which grow on top. The defence grows in response to predator cues (kairomones) released by midge larvae predators (Chaoborus spp., Parejko & Dodson, 1991;Tollrian, 1993), starting with the development of the neck-pedestal, which first begins to grow during the late embryonic stage at the onset of kairomone sensitivity, followed by the defensive head spikes which develop later in the early juvenile stages (Naraki et al., 2013;Weiss et al., 2016). The maintenance of the defence requires consistent exposure to predator cues (Imai et al., 2009) and usually lasts until the third instar, after which the Daphnia are large enough to escape size-selective predation (Tollrian, 1993). ...
Predator-induced shape plasticity in Daphnia pulex
Article
Full-text available
  • Feb 2024
All animals and plants respond to changes in the environment during their life cycle. This flexibility is known as phenotypic plasticity and allows organisms to cope with variable environments. A common source of environmental variation is predation risk, which describes the likelihood of being attacked and killed by a predator. Some species can respond to the level of predation risk by producing morphological defences against predation. A classic example is the production of so‐called ‘neckteeth’ in the water flea, Daphnia pulex , which defend against predation from Chaoborus midge larvae. Previous studies of this defence have focussed on changes in pedestal size and the number of spikes along a gradient of predation risk. Although these studies have provided a model for continuous phenotypic plasticity, they do not capture the whole‐organism shape response to predation risk. In contrast, studies in fish and amphibians focus on shape as a complex, multi‐faceted trait made up of different variables. In this study, we analyse how multiple aspects of shape change in D. pulex along a gradient of predation risk from Chaoborus flavicans . These changes are dominated by the neckteeth defence, but there are also changes in the size and shape of the head and the body. We detected change in specific modules of the body plan and a level of integration among modules. These results are indicative of a complex, multi‐faceted response to predation and provide insight into how predation risk drives variation in shape and size at the level of the whole organism.
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... Since we could not obtain a sufficient amount of RNA from one individual, we pooled the experimental individuals. As embryos contain high amounts of RNA and can perceive predator cues, we accounted for the stage of egg development within the brood pouch [77]. Because sampling females in the inter-molt stage can ensure stable gene expression, only egg-bearing experimental females were pooled [77]. ...
... As embryos contain high amounts of RNA and can perceive predator cues, we accounted for the stage of egg development within the brood pouch [77]. Because sampling females in the inter-molt stage can ensure stable gene expression, only egg-bearing experimental females were pooled [77]. ...
Comparative transcriptome analysis of two Daphnia galeata genotypes displaying contrasting phenotypic variation induced by fish kairomones in the same environment of the Han River, Korea
Article
Full-text available
  • Oct 2023
  • BMC GENOMICS
Background Phenotypic plasticity is a crucial adaptive mechanism that enables organisms to modify their traits in response to changes in their environment. Predator-induced defenses are an example of phenotypic plasticity observed across a wide range of organisms, from single-celled organisms to vertebrates. In addition to morphology and behavior, these responses also affect life-history traits. The crustacean Daphnia galeata is a suitable model organism for studying predator-induced defenses, as it exhibits life-history traits changes under predation risk. To get a better overview of their phenotypic plasticity under predation stress, we conducted RNA sequencing on the transcriptomes of two Korean Daphnia galeata genotypes, KE1, and KB11, collected in the same environment. Results When exposed to fish kairomones, the two genotypes exhibited phenotypic variations related to reproduction and growth, with opposite patterns in growth-related phenotypic variation. From both genotypes, a total of 135,611 unigenes were analyzed, of which 194 differentially expressed transcripts (DETs) were shared among the two genotypes under predation stress, which showed consistent, or inconsistent expression patterns in both genotypes. Prominent DETs were related to digestion and reproduction and consistently up-regulated in both genotypes, thus associated with changes in life-history traits. Among the inconsistent DETs, transcripts encode vinculin (VINC) and protein obstructor-E (OBST-E), which are associated with growth; these may explain the differences in life-history traits between the two genotypes. In addition, genotype-specific DETs could explain the variation in growth-related life-history traits between genotypes, and could be associated with the increased body length of genotype KE1. Conclusions The current study allows for a better understanding of the adaptation mechanisms related to reproduction and growth of two Korean D. galeata genotypes induced by predation stress. However, further research is necessary to better understand the specific mechanisms by which the uncovered DETs are related with the observed phenotypic variation in each genotype. In the future, we aim to unravel the precise adaptive mechanisms underlying predator-induced responses.
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... Agrawal et al., 1999;Keiser and Mondor, 2013;Luquet and Tariel, 2016;Stein et al., 2018). To our knowledge, only four experiments have studied the sensitive windows of WGP on inducible defences using Hyla versicolor tadpoles (Rick A. Relyea, 2003), Helisoma trivolvis freshwater snails (Hoverman and Rick A. Relyea, 2007), Daphnia magna water fleas (Mikulski et al., 2005), Daphnia longicephala Juliette water fleas (Weiss et al., 2016); and only one experiment has studied the sensitive windows of TGP of inducible defences using Daphnia magna (Mikulski and Pijanowska, 2010). The aim of our study was to determine the sensitive windows of WGP and TGP using the example of inducible defences in the freshwater snail Physa acuta. ...
... The results also provide evidence that there were several sensitive windows (Embryo, Early and Late) that induced higher resistance of shells against crush. The results thus demonstrated that the developmental window of cue exposure is an important factor driving anti-predator within-generational responses in line with the literature in other species (Hoverman and Rick A. Relyea, 2007;Mikulski et al., 2005;Rick A. Relyea, 2003;Weiss et al., 2016). Our results confirmed our prediction that early stages are highly sensitive to the environment, here P. acuta embryos are able to detect predator cues, but also highlighted that the later stages are sensitive. ...
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... Subsequent studies have found that embryos in a wide range of taxa are able to respond to acoustic cues and, in some cases, it has been shown that exposure to those cues as embryos results in adaptive changes in the subjects' developmental trajectories after birth or hatching (review in Mariette et al. 2021). Other examples of situations in which individuals begin to be sensitive to cues from the external environment prior to birth or hatching include Daphnia embryos that are sensitive to chemical cues produced by predators (Weiss et al. 2016) and treefrog embryos that are sensitive to tactile cues indicative of predators (Warkentin 2005). ...
... However, when the Daphnia have grown too large for Chaoborus to consume them, they no longer produce those defensive structures. Hence, as one would expect, Daphnia begin to be sensitive to cues from Chaoborus when they are embryos (Weiss et al. 2016), and they cease to be sensitive to those cues when they approach the sizes at which they are no longer vulnerable to that predator (Imai et al. 2009). ...
Sensitive Period Diversity: Insights From Evolutionary Models
Article
  • Dec 2022
Recent models of the evolution of sensitive periods in response to informative stimuli (i.e., cues) provide insights into reasons why empiricists within and across disciplines might observe variation in the patterns they observe when they study sensitive periods. We consider what an evolutionary perspective can tell us about the appropriate age to begin and end a study of sensitive periods, and how the experimental design and the predispositions of the subjects in an empirical study might affect its results. Using models based on Bayesian updating, we show how several factors, including the protocol used to study sensitive periods, the relative reliability of the information provided to the subjects, and the predispositions of the subjects, are expected to affect the presence and shapes of sensitive periods that occur in response to information-only cues. Our results suggest that investigators will observe considerable variation in the patterns reported in empirical studies of sensitive periods simply based on the protocol they use to study them; this is relevant because investigators working in different disciplines tend to rely on different protocols. We show how theory can help shed light on the adaptive significance of patterns reported by empiricists, e.g., why we might expect to observe heightened sensitivity to particular cues during adolescence. We describe existing empirical support for some of the models’ predictions, e.g., that theduration of sensitive periods will be extended if subjects are first maintained in noninformative conditions before they are first exposed to informative stimuli. We highlight novel predictions of these models that can be readily tested by empiricists, e.g., that the effects of deprivation treatments on sensitive periods will vary, depending on their timing. More generally, we show how an evolutionary approach to sensitive periods reveals that at least some of the considerable variation observed in the results reported in empirical studies of sensitive periods may be attributable to variation in the methods that are used to study them
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... Sampling females in the intermolt stage ensures stable gene expression; therefore, only egg-bearing experimental females were pooled. [34]. Total RNA was isolated using the Qiagen RNeasy Plus Universal Mini Kit (Qiagen, Valencia, CA, USA) following the manufacturer's instructions after homogenization with a disposable pestle and homogenizer. ...
Differences in alternative splicing events in the adaptive strategies of two Daphnia galeata genotypes induced by fish kairomones
Article
Full-text available
  • Jul 2024
  • BMC GENOMICS
Background Daphnia galeata is a suitable model organism for investigating predator-induced defense. Genes and pathways exhibiting differential expression between fish kairomone-treated and untreated groups in D. galeata have been identified. However, understanding of the significance of alternative splicing, a crucial process of the regulation of gene expression in eukaryotes, to this mechanism remains limited. This study measured life-history traits and conducted short-read RNA sequencing and long-read isoform sequencing of two Korean D. galeata genotypes (KB1 and KE2) to uncover the genetic mechanism underlying their phenotypic plasticity under predation stress. Results KB1 exhibited strategies to enhance fertility and decrease body length when exposed to fish kairomones, while KE2 deployed an adaptive strategy to increase body length. Full-length transcriptomes from KB1 and KE2 yielded 65,736 and 57,437 transcripts, respectively, of which 32 differentially expressed transcripts (DETs) were shared under predation stress across both genotypes. Prominent DETs common to both genotypes were related to energy metabolism and the immune system. Additionally, differential alternative splicing (DAS) events were detected in both genotypes in response to fish kairomones. DAS genes shared between both genotypes may indicate their significant role in the post-transcriptional stress response to fish predation. Calpain-3, involved in digestion and nutrient absorption, was identified as a DAS gene in both genotypes when exposed to fish kairomones. In addition, the gene encoding thymosin beta, which is related to growth, was found to be a statistically significant DAS only in KB1, while that encoding ultraspiracle protein, also associated with growth, was only identified in KE2. Moreover, transcripts encoding proteins such as EGF-like domain-containing protein, vitellogenin fused with superoxide dismutase, and others were identified overlapping between DAS events and DETs and potentially elucidating their association with the observed phenotypic variation in each genotype. Conclusions Our findings highlight the crucial role of alternative splicing in modulating transcriptome landscape under predation stress in D. galeata, emphasizing the requirement for integrating gene expression and splicing analyses in evolutionary adaptation studies.
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Variation in defensive spines across juvenile instars of Daphnia magna
Article
  • Jul 2024
Various species of freshwater zooplankton feature defensive spines, spikes or spinules across a comparatively wide size range. Among those is Daphnia magna, which has previously been found to express an enhanced spinescence in response to the predatory tadpole shrimp Triops cancriformis. This involves an elongated tail-spine, further protruding fornices and elongated, as well as further spread spinules along its carapace margins. Of these, the predator-induced trait changes concerning the spinules of D. magna at the age of first reproduction are known. However, their morphological development throughout the juvenile instars, in comparison to the changes of the prominent tail spine during the same periods, has thus far been unclear. Our study shows that D. magna expresses spinules across all investigated juvenile instars. Furthermore, during ontogeny, the development of D. magna’s rather small spinescence traits, i.e. the dorsal and ventral mean spinule length, as well as the dorsal spinules bearing area, in response to predation pressure, differs distinctly from that of the prominent tail-spine. Thus, our study provides further insight into the connectedness of traits contributing to the overall defensively enhanced spinescence of D. magna, with possible implications for the functional benefit of the traits at certain developmental periods.
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Persistent and sex-independent effects of decreased calcium concentration inhibiting morphological defense of Daphnia: Evidences from morphological traits and expression of the associated genes
Article
  • Mar 2023
  • SCI TOTAL ENVIRON
The continuous decline in calcium concentration in freshwater as a widespread environmental stress can have complex effects on the interspecific relationships of organisms, such as interference with the anti-predation defenses of Daphnia with high calcium demand. The natural population of Daphnia includes individuals with different developmental stages and sexes. Here, we measured the effects of decreased calcium concentration on morphological defense of Daphnia after different numbers of molts or under various sexes and the expression of genes related to signal recognition, carapace formation, reproductive allocation, and stress defense. Results showed that decreased Ca concentration resulted in the altered effects of fish kairomone on the change rates of body size, change rates of spine length, and change rates of relative spine length disappear. Furthermore, male Daphnia also developed morphological defense under fish predation risk, which was also inhibited by decreased Ca concentration, but no significant difference was observed in the intensity of induced defense between male and female Daphnia at low Ca concentrations. Importantly, decreased Ca concentrations did not alter the increase in expressions of genes related to neural signaling by fish kairomone. Fish kairomone promoted the expression of reproduction-related genes, whereas decreased Ca concentration inhibited their expression. Fish kairomone altered the expression of carapace-related genes, but most were disturbed by decreased Ca concentration. Decreased Ca concentration inhibited the increased expression of stress defense-related genes by fish kairomone. This study contributes to a more comprehensive understanding of the effects of environmental changes on interspecific relationships among aquatic organisms of different developmental stages and different sexes.
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Sensitive windows for within- and trans-generational plasticity of anti-predator defences
Preprint
Full-text available
  • Nov 2022
Trans-generational plasticity could be an important mechanism for adaptation to variable environments in addition to within-generational plasticity. But its potential for adaptation may be restricted to specific developmental windows that are highly sensitive and responsive to environmental changes. Determining these sensitive windows is essential to understand the temporal dynamic of environmental change detection, phenotype induction and selection. We examined the sensitive windows of both within- and trans-generational plasticity of anti-predator defences in the freshwater snail Physa acuta. Parental snails were exposed to olfactory cues of crayfish predator at different exposure windows: embryonic development, early, mid or late post-embryonic development. Behavioural and morphological defences were then assessed in adult parents and offspring. Overall, none of the exposure windows was particularly sensitive compared to the others. The sensitive window for within- and trans-generational defence induction was thus very wide, which could be the result of the strong selective pressure imposed by predation at all developmental stages. Although all exposure windows impacted on the expression of offspring defences, they did so differently and the response patterns were complex for morphological offspring defences. This complexity in the temporal dynamics of transgenerational induction could result from the transmission to offspring of both cues about predator presence and parental somatic condition.
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Performance of Daphnia simultaneously exposed to nitrite and predation risk: Reduced nitrite tolerance and aggravated predation-induced miniaturization
Article
  • Nov 2022
  • SCI TOTAL ENVIRON
Nitrogenous pollutants derived from human activities not only pose direct risk on aquatic organisms but may also indirectly endanger the stability of interspecific relations. To date, the effects of the nitrogen-containing pollutants on the induced defense remain unclear. Here, we aim to investigate the induced defense of an aquatic keystone species, Daphnia pulex, which responds to predation risk under nitrite pollution at environmentally relevant concentrations and simultaneously evaluate the effects of their induced defenses on nitrite tolerance. Results showed that increasing nitrite significantly reduced the survival time of D. pulex and posed severe reproductive toxicity, consequently reducing the offspring and broods. In the morphological defensive responses, early nitrite exposure interfered with the spine elongation, but the relative spine length induced by the predation risk was unaffected by the nitrite concentrations with exposure time prolonged, although high-dose nitrite inhibited the spine elongation and the increase of the body size. The integration of biomarker response index analyses further indicated that the reproductive capacity was more seriously impaired than the morphology and the survival. Moreover, the sensitivity analyses of growth and reproduction indicated that predation risk significantly reduced Daphnia's tolerance to nitrite. Conclusively, these findings highlight that long-term nitrite exposure exacerbates the predator-induced miniaturization of zooplanktons, and predation risk also reduces their tolerance to nitrite, which provides new insights into the performance changes of zooplanktons exposed to pollutants under predation risk and the vulnerability of predator–prey interspecific relationships in polluted environments.
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Predator-induced defences in Daphnia longicephala: Location of kairomone receptors and timeline of sensitive phases to trait formation
Article
Full-text available
  • Sep 2015
  • J EXP BIOL
The freshwater crustacean Daphnia adapts to changing predation risks by forming inducible defences. These are only formed when they are advantageous, saving associated costs when the defence is superfluous. However, in order to be effective, the time lag between the onset of predation and the defence formation has to be short. Daphnia longicephala develop huge protective crests upon exposure to chemical cues (kairomones) from its predator the heteropteran backswimmer Notonecta glauca. To analyse time lags, we determined kairomone-sensitive stages and the developmental time frames of inducible defences. Moreover, we looked at additive effects that could result from the summation of prolonged kairomone exposure. Kairomones are perceived by chemoreceptors and integrated by the nervous system, which alters the developmental program leading to defence formation. The underlying neuronal and developmental pathways are not thoroughly described and surprisingly, the location of the kairomone receptors is undetermined. We show that D. longicephala start to sense predator cues at the onset of the second juvenile instar, defences develop with a time lag of one instar and prolonged kairomone exposure does not impact the magnitude of the defence. By establishing a method to reversibly impair chemosensors, we show the first antennae as the location of kairomone-detecting chemoreceptors. This study provides fundamental information on kairomone perception, kairomone-sensitive stages, developmental time frames and lag times of inducible defences in D. longicephala that will greatly contribute to the further understanding of the neuronal and developmental mechanisms of predator-induced defences in Daphnia.
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Predator-Induced Morphological Defenses: Costs, Life History Shifts, and Maternal Effects in Daphnia Pulex
Article
  • Sep 1995
This study was designed to measure and separate the physiological costs of inducible defenses from life history trade-offs and maternal effects in the waterflea Daphnia pulex. Juveniles of D. pulex produce morphological changes (@'neckteeth@') and undergo life history shifts as defenses against predatory Chaoborus (phantom midge) larvae. These traits are induced by a chemical cue (kairomone) released by the predator. I performed life history experiments with and without Chaoborus kairomones at different food levels to quantify the induced changes and their potential physiological costs. The Daphnia clone used in this study also increased its body depth in response to the predator substance. Life history shifted toward a larger body size (both length and depth) and higher fecundity, which was balanced by an increased time to reach maturity and by increased adult instar durations. Reproductive effort was higher in the typical morph in the first adult instar, indicating resource allocation shifts towards growth in the protected morph. However, even in the absence of predation the chemically induced protected morph tended to show an increased intrinsic rate of population growth (r). The longer time to reach maturity was not a direct physiological cost of neckteeth production, but a trade-off for larger body size. The life history shifts are independent of neckteeth formation. Developmental mechanisms leading to life history changes occurred after neckteeth were induced and could thus be uncoupled from neckteeth formation and its direct costs. In this study no direct costs were found. Carbon incorporation rates for the two morphs, at high and low food, were not different. As a maternal effect, the large females of the induced morph produced larger neonates which, in turn, matured at a larger size. Morphological changes, life history shifts, and maternal effects acted in concert to form defenses against Chaoborus. This study shows that the often assumed high physiological costs resulting from the formation or maintenance of the defenses are not necessary to explain the evolution of inducible defenses. As morphological changes increase the visibility of Daphnia pulex, a fitness disadvantage can be caused by a changing predator regime (e.g., fish). The results of this study suggest that environments with changing predator selectivities favor the evolution of inducible defenses.
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Identification of the Precise Kairomone-sensitive Period and Histological Characterization of Necktooth Formation in Predator-induced Polyphenism in Daphnia pulex
Article
  • Aug 2013
Many organisms have the ability to alter their development in the presence of predators, leading to predator-induced defenses that reduce vulnerability to predation. In the water flea Daphnia pulex, small protuberances called 'neckteeth' form in the dorsal neck region in response to kairomone(s) released by predatory phantom midges (Chaoborus larvae). Although previous studies suggested that kairomone sensitivity begins when chemoreceptors begin to function during embryogenesis, the exact critical period was unknown to date. In this study, we investigated the period of kairomone sensitivity and the process of necktooth formation in D. pulex through extensive treatments with pulses of kairomone(s). First, we described the time course of embryogenesis, which we suggest should be used as the standard in future studies. We found the kairomone-sensitive period to be relatively short, extending from embryonic stage 4 to postembryonic first instar. We observed cell proliferation and changes in cell structure in response to the kairomone treatment, and propose a model for necktooth formation. Preliminary LiCl treatment suggests the Wnt signaling pathway involved in crest formation as a candidate for the molecular mechanism underlying this process. Our study provides basic insight toward understanding the mechanisms underlying adaptive polyphenism in D. pulex.
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Embryological induction and predation ecology in Daphnia pulex
Article
  • Mar 1981
Abstract Results of laboratory,experiments,suggest,that a water-soluble,factor released,into the en- vironment,by,the,predacious,phantom,midge,larva,Chaoborus,americanus,(Diptera: Cha- oboridae),causes,embryos,of the water-flea Daphnia,pulex,Leydig,1860 emend.,Richard,1896 (Crustacea: Cladocera),to develop,into a form,called,Daphnia,minnehaha,Herrick,1884. Chaoborus,larvae,are unable,to eat the D. minnehaha,form,as readily,as the D. pulex,form. Many,planktonic,cladoceran,popula- tions are either polymorphic,or undergo some,sort,of,seasonal,change,in,form. Several workers,have,recently,found,that the,different,forms,experience,different degrees,of mortality,in the,presence,of invertebrate,predators,(Zaret 1972; Dod- son,1974a; Kerfoot,1977; O’Brien and Vinyard,1978; O’Brien et al. 1979). In an analogous system, embryos of the plank- tonic,rotifer,Brachionus,cal ycijlorus,re- spond,to a chemical,released,by,the pre- dacious,rotifer Asplanchna,by developing a,spiny,form,which,is resistant,to As- planchna,predation,(Gilbert 1966). IIow- ever, no such system has previously been found,for a,crustacean,(but see,Grant and,Bayly,1981). Our,study,offers,evi- dence,that,the,predatory,midge,larva Chaoborus,americanus,releases,into,its environment,a chemical,that induces,the embryological,development,of a predator- resistant,form,of Daphnia,pulex. The,resistant,offspring,of a,D. pulex mother,are,morphologically,indistin-
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Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity: Morphological effects of Chaoborus kairomone concentration and their quantification
Article
  • Nov 1993
Many clones of Daphnia pulex develop morphological changes as antipredator devices in the presence of chemicals released by Chaoborus larvae. The D.pulex clone used in this experiment develops neckteeth until the end of the fourth juvenile instar when exposed to chemical cues from Chaoborus flavicans. This clone develops small neckteeth in the first instar even when it has not been exposed to the chemicals. Neckteeth formation is a continuous process that involves changes in the whole neck region. On the basis of these changes, a scoring method is presented that allows easy classification of the morphological changes. Neckteeth formation was strongest in the second juvenile instar, followed by a slightly weaker response in the third juvenile instar. Neckteeth formation within one instar is concentration dependent and exhibits a saturation curve. The maintenance of neckteeth over several instars is also concentration dependent. At low kairomone concentrations, neckteeth were restricted to the first two instars. This study indicates that neckteeth formation in successive instars is different, probably to optimize costs and benefits by equalizing or reducing vulnerability in successive juvenile instars at different Chaoborus densities.
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