11 research outputs found
Inducible Defenses with a "Twist": Daphnia barbata Abandons Bilateral Symmetry in Response to an Ancient Predator
Predation is one of the most important drivers of natural selection. In consequence a huge variety of anti-predator defenses have evolved in prey species. Under unpredictable and temporally variable predation pressure, the evolution of phenotypically plastic defensive traits is favored. These "inducible defenses", range from changes in behavior, life history, physiology to morphology and can be found in almost all taxa from bacteria to vertebrates. An important group of model organisms in ecological, evolutionary and environmental research, water fleas of the genus Daphnia (Crustacea: Cladocera), are well known for their ability to respond to predators with an enormous variety of inducible morphological defenses. Here we report on the "twist", a body torsion, as a so far unrecognized inducible morphological defense in Daphnia, expressed by Daphnia barbata exposed to the predatory tadpole shrimp Triops cancriformis. This defense is realized by a twisted carapace with the helmet and the tail spine deviating from the body axis into opposing directions, resulting in a complete abolishment of bilateral symmetry. The twisted morphotype should considerably interfere with the feeding apparatus of the predator, contributing to the effectiveness of the array of defensive traits in D. barbata. As such this study does not only describe a completely novel inducible defense in the genus Daphnia but also presents the first report of a free living Bilateria to flexibly respond to predation risk by abandoning bilateral symmetry
Modality matters for the expression of inducible defenses: introducing a concept of predator modality
Background: Inducible defenses are a common and widespread form of phenotypic plasticity. A fundamental factor driving their evolution is an unpredictable and heterogeneous predation pressure. This heterogeneity is often used synonymously to quantitative changes in predation risk, depending on the abundance and impact of predators. However, differences in `modality', that is, the qualitative aspect of natural selection caused by predators, can also cause heterogeneity. For instance, predators of the small planktonic crustacean Daphnia have been divided into two functional groups of predators: vertebrates and invertebrates. Predators of both groups are known to cause different defenses, yet predators of the same group are considered to cause similar responses. In our study we question that thought and address the issue of how multiple predators affect the expression and evolution of inducible defenses. Results: We exposed D. barbata to chemical cues released by Triops cancriformis and Notonecta glauca, respectively. We found for the first time that two invertebrate predators induce different shapes of the same morphological defensive traits in Daphnia, rather than showing gradual or opposing reaction norms. Additionally, we investigated the adaptive value of those defenses in direct predation trials, pairing each morphotype (non-induced, Triops-induced, Notonecta-induced) against the other two and exposed them to one of the two predators. Interestingly, against Triops, both induced morphotypes offered equal protection. To explain this paradox we introduce a `concept of modality' in multipredator regimes. Our concept categorizes two-predator-prey systems into three major groups (functionally equivalent, functionally inverse and functionally diverse). Furthermore, the concept includes optimal responses and costs of maladaptions of prey phenotypes in environments where both predators co-occur or where they alternate. Conclusion: With D. barbata, we introduce a new multipredator-prey system with a wide array of morphological inducible defenses. Based on a `concept of modality', we give possible explanations how evolution can favor specialized defenses over a general defense. Additionally, our concept not only helps to classify different multipredator-systems, but also stresses the significance of costs of phenotype-environment mismatching in addition to classic `costs of plasticity'. With that, we suggest that `modality' matters as an important factor in understanding and explaining the evolution of inducible defenses
Modality matters for the expression of inducible defenses: introducing a concept of predator modality
Reversibility of inducible defenses in Daphnia
Nahezu jeder Organismus ist im engeren oder weiteren Sinne PrĂ€dation ausgesetzt, sei es durch PrĂ€datoren sensu strictu, WeidegĂ€nger, Parasiten oder Parasitoiden. Da jedoch der PrĂ€dationsdruck hĂ€ufig Schwankungen und VerĂ€nderungen unterliegt, werden eine groĂe Anzahl an Anpassungen auf diese Bedrohung plastisch im PhĂ€notyp ausgeprĂ€gt. Diese sogenannten induzierbaren Verteidigungen finden sich weit verbreitet in nahezu allen gröĂeren Taxa. Sie ermöglichen einen Schutz bei vorhandener Bedrohung, wĂ€hrend sie in Abwesenheit selbiger nicht ausgebildet werden und infolgedessen mit der Expression verbundene Kosten einsparen. Ein weiterer Schritt in der PlastizitĂ€t ist das ZurĂŒckbilden einmal induzierter Verteidigungen. Essentiell dafĂŒr sind jedoch Kosten, die nach Ausbildung weiterhin bestehen, etwa durch Aufrechterhaltung der Verteidigung oder Maladaptation an die verĂ€nderte Umwelt. Theoretische Studien lassen vermuten, dass eine solche ReversibilitĂ€t ein hĂ€ufiges PhĂ€nomen darstellt. Bislang bestehen dafĂŒr allerdings mit Ausnahme von verhaltens-basierten Verteidigungen nur wenige experimentelle Nachweise. Dies trifft insbesondere auf die induzierbaren Verteidigungen innerhalb der Gattung Daphnia zu. Diese Gruppe von Modellorganismen der limnologischen, ökotoxikologischen und bio-medizinischen Forschung liefert zahlreiche Beispiele induzierbarer Verteidigungen durch Ănderungen in Verhalten, Life-History sowie Morphologie. Insbesondere letztere sind als PhĂ€nomen der âZyklomorphoseâ seit ĂŒber hundert Jahren bekannt, mit einem starken Fokus der Forschung in den letzten Jahrzehnten und infolgedessen der Beschreibung zahlreicher, weiterer Beispiele. Dennoch ist ĂŒber ReversibilitĂ€t induzierbarer Verteidigungen innerhalb der Gattung Daphnia bislang kaum etwas bekannt. Selbiges gilt auch fĂŒr den Einfluss von mit induzierbaren Verteidigungen assoziierten Kosten in Bezug auf die ReversibilitĂ€t phĂ€notypischer Anpassungen sowie möglicher physiologischer EinschrĂ€nkungen.Die Rolle und Bedeutung ökologischer Faktoren, wie etwa Unterschiede in den RĂ€ubern, wurde darĂŒber hinaus ebenfalls bislang nicht untersucht. Ziel dieser Promotion war daher die Identifikation von ReversibilitĂ€t induzierbarer Verteidigungen innerhalb der Gattung Daphnia mit einem Fokus auf morphologische Parameter. FĂŒr die Unterscheidung von physiologischen und ökologischen Faktoren wurde die Etablierung eines neuen Systems mit mehreren RĂ€ubern angestrebt. Des Weiteren wurde ReversibilitĂ€t ebenfalls in einem etablierten System untersucht. DarĂŒber hinaus sollte die Bedeutung von Kosten induzierbarer Verteidigungen in Bezug auf die ReversibilitĂ€t untersucht werden.
Basierend auf der afrikanischen Art Daphnia barbata sowie den beiden invertebraten PrĂ€datoren Triops cancriformis und Notonecta glauca, wurde ein neues System entdeckt, beschrieben und fĂŒr die Untersuchung auf ReversibilitĂ€t herangezogen. Dabei konnten in einer Studie erstmals induzierbare Verteidigungen fĂŒr diese Art nachgewiesen werden. Infolgedessen zeigte sich, dass D. barbata auf Basis derselben Strukturen, unterschiedliche, auf die jeweiligen RĂ€uber angepasste, spezialisierte Verteidigungen ausbildet. Starke Maladaptationskosten konnten mittels direkter PrĂ€dationsversuche mit vertauschten RĂ€ubern jedoch bei keiner der beiden induzierten Morphotypen beobachtet werden. Einige der vorgefundenen Anpassungen stellen zudem bislang gĂ€nzlich unbeschriebene morphologische Verteidigungen innerhalb der Gattung Daphnia dar. Darunter fĂ€llt insbesondere die Körpertorsion durch Triops-Induktion, die zu einem Verlust der Bilateral-Symmetrie fĂŒhrt. DarĂŒber hinaus wurde ein theoretisches Konzept beschrieben, das den Einfluss multipler PrĂ€datoren fĂŒr die auf Beuteorganismen wirkende natĂŒrliche Selektion und die erwartete phĂ€notypische Expression induzierter Verteidigungen beschreibt. Des Weiteren wurde mittels des Konzeptes eine Kategorisierung von Multi-PrĂ€dator-Systemen vorgenommen, basierend auf der Vektorisierung von SelektionsdrĂŒcken. In einer weiteren Studie wurde gezeigt, dass sowohl Torsion sowie, mit Ausnahme der HelmgröĂe, die Mehrzahl induzierter morphologischer Verteidigungen gegen Triops reversibel sind. GegenĂŒber Notonecta ausgebildete morphologische VerĂ€nderungen wurden hingegen nicht zurĂŒckgebildet, selbst solche nicht, die bei beiden induzierten Morphotypen auftraten. Damit konnte erstmalig experimentell gezeigt werden, dass zwar physiologische Faktoren die ReversibilitĂ€t induzierbarer Verteidigungen in Daphnien beeinflussen können, dass aber ökologische Faktoren ebenfalls eine hohe Relevanz besitzen. Zur Identifikation von ReversibilitĂ€t in einem etablierten System wurde die Art Daphnia magna als Beuteorganismus, sowie T. cancriformis als RĂ€uber herangezogen. Hierbei konnte bei adulten induzierten Tieren eine starke ReversibilitĂ€t von morphologischen sowie von Life-History Parametern innerhalb weniger HĂ€utungen beobachtet werden. Ebenso zeigte sich erstmals, dass selbst bei adulten D. magna noch Verteidigungen induziert werden können. In einer weiteren Studie wurden mögliche kontinuierliche Kosten untersucht, die im Zusammenhang mit der Schwimmeffizienz stehen. TatsĂ€chlich konnte gezeigt werden, dass induzierte D. magna eine deutlich erhöhte Absinkgeschwindigkeit aufweisen.Schwimmexperimente wiesen jedoch darauf hin, dass diese Unterschiede von induzierten Tieren vollstĂ€ndig kompensiert werden. Weitere Berechnungen legen zudem nahe, dass mit weniger als 0,1% des Energiehaushaltes der energetische Aufwand der Kompensation ĂŒberaus gering ausfĂ€llt. In Bezug auf die dennoch beobachtete ReversibilitĂ€t könnte dies auf weitere, bislang verborgene Kosten hinweisen, etwa durch das mit der HĂ€utung verbundene zyklische Erneuern der Verteidigungen.
Die in dieser Dissertation beschriebenen Ergebnisse liefern damit die ersten klaren Nachweise von ReversibilitĂ€t induzierbarer morphologischer Verteidigungen, eine EinschĂ€tzung zu den verbundenen Kosten und die Beschreibung bislang unbekannter induzierbarer Verteidigungen. DarĂŒber hinaus wurde ein neues Multi-RĂ€uber-Beute-System mit einer weiterfĂŒhrenden Grundlage zu proximaten und ultimaten Faktoren von ReversibilitĂ€t beschrieben.Almost every organism is subject to predation, may it be through predators sensu strictu, grazers, parasites or parasitoids. Since predation pressure often undergoes changes and variations, a large number of adaptations to this threat are plastic in their phenotype. These so-termed inducible defenses are widespread in almost all larger taxa. They allow protection if a threat is present, while they are not being expressed in its absence, thus saving associated costs. Another level of plasticity is the reversion of already induced defenses. However, for reversibility costs are essential, that remain after the expression of the defense, such as for its maintenance or through maladaptation to the new environment. Theoretical studies suggest, that reversibility is a common phenomenon. Still, with the exception of behavior-based defenses, only few experimental records exist. This applies especially to the genus Daphnia. This group of model organisms of limnological, eco-toxicological and bio-medical research provides numerous examples for inducible defenses through changes in behavior, life-history and morphology. The latter has been known as âcyclomorphosisâ for over a hundred years, with recent attention in the last decades, leading to a growing number of described inducible defenses. However, despite this focus, almost nothing is known about the reversibility of inducible defenses in the genus Daphnia. The same applies to the influence of costs and limitations on the reversibility of induced defenses and the underlying physiological and ecological factors. Therefore, the aim of this thesis was the identification of reversibility of inducible defenses within the genus Daphnia, with a focus on morphological parameters. Furthermore, the establishment of a new multi-predator-prey system was proposed, in order to achieve a differentiation between physiological and ecological factors influencing reversibility. An already established predator-prey system was to be used for additional tests of reversibility. Finally, within the scope of this thesis was to assess possible costs of inducible defenses in relation to their reversibility.
Based on the African species Daphnia barbata and the two invertebrate predators Triops cancriformis and Notonecta glauca, a new system was discovered, described and used to test for reversibility. This led to the first description of inducible defenses in this species. Additionally, it was shown that D. barbata induces defenses based on the same structures, but distinctly adapted to each of the two predators. Strong maladaptation costs could not be found for either of the two defensive morphotypes, when exposing them to the mismatching predator in predation trials. Furthermore, some of the defensive traits of D. barbata are previously undescribed morphological defenses in the genus Daphnia, most notably the body torsion, which leads to an abolishment of bilateral symmetry. In addition, a theoretical framework was developed in order to explain how multiple predators affect the selection pressure acting on prey organisms as well as the resulting expression of inducible defenses in the phenotype. This framework was then used for a categorization of multi-predator systems based on the vectorization of selection pressures. In a further study, it was shown that with the exception of helmet size, the majority of morphological defenses against Triops â including body torsion - are reversible. On the contrary, induced morphological defenses against Notonecta were not reverted â not even traits, that both defended morphotypes shared. In consequence, for the first time it could be shown experimentally that, while physiological factors hold an influence, ecological factors have a high importance for the reversibility of inducible defenses or the lack therof. Regarding the identification of reversibility in an established system, the species Daphnia magna was used as prey organism together with the predator T. cancriformis. It could be shown, that adult induced D. magna can revert both morphological and life-history defenses within a short timeframe. Similarly, an induction of previously non-induced adult daphnids could be described. Using the same predator-prey system, potential running costs associated with inducible defenses and swimming efficiency were tested for in a further study. It was determined, that induced D. magna possessed a larger drag and consequently higher sinking rate compared to non-induced daphnids of the same size. However, swimming experiments showed that induced D. magna compensate these differences fully. Furthermore, calculations suggest that the energetic costs of this compensation only amounts to approximately 0.01% of the general energy consumption of the daphnids. In relation to the observed reversibility in D. magna, this could hint at hidden costs, e.g. through the periodical renewal of inducible defenses in connection with the molting process.
In conclusion, this thesis provides not only the first substantial records of reversibility of inducible morphological defenses, but also an estimation of associated costs and the description of previously unknown inducible defenses. Finally, a new multi-predator-prey system is presented together with groundwork for the estimation of proximate and ultimate causes and conditions for the phenomenon of reversibility of inducible defenses
Comparison of the body torsion in non-predator-exposed (Control) and predator-exposed (Induced) primiparous <i>Daphnia barbata</i>.
<p>Body torsion is here defined as the sum of helmet and tail spine deviation from the body axis. The error bars show the standard error of Mean (SE), the asterisks indicate the significance level (*** <i>P</i> < 0.001) based on a F-Test (<i>F</i>(1, 22) = 264.09).</p
Scanning electron microscope images of the experimental animals.
<p>a) <i>Triops cancriformis</i>, ventral view with the arrow pinpointing to the narrow food groove. The ancient predator feeds on <i>Daphnia</i>, which are caught, subsequently placed into the food groove and transported towards the mandibles; b) Dorsal view of a <i>Triops</i>-exposed morph of <i>Daphnia barbata</i> showing the âtwistedâ appearance. The tips of helmet and tail spine deviate from the body axis in opposite directions, leading to an S-shaped dorsal ridge and thus abolishing bilateral symmetry of the individual. The twisted morphotype can be assumed to severely impede the transport through the food groove as it should cause the daphnid to wedge within the food groove of the predator. c) Dorsal view of <i>D</i>. <i>barbata</i> not exposed to the predator. The dorsal ridge aligns with the bilateral body axis, the tips of helmet and tail spine do not deviate from the body axis.</p
Inducible Defenses with a "Twist": <i>Daphnia barbata</i> Abandons Bilateral Symmetry in Response to an Ancient Predator
<div><p>Predation is one of the most important drivers of natural selection. In consequence a huge variety of anti-predator defenses have evolved in prey species. Under unpredictable and temporally variable predation pressure, the evolution of phenotypically plastic defensive traits is favored. These âinducible defensesâ, range from changes in behavior, life history, physiology to morphology and can be found in almost all taxa from bacteria to vertebrates. An important group of model organisms in ecological, evolutionary and environmental research, water fleas of the genus <i>Daphnia</i> (Crustacea: Cladocera), are well known for their ability to respond to predators with an enormous variety of inducible morphological defenses. Here we report on the âtwistâ, a body torsion, as a so far unrecognized inducible morphological defense in <i>Daphnia</i>, expressed by <i>Daphnia barbata</i> exposed to the predatory tadpole shrimp <i>Triops cancriformis</i>. This defense is realized by a twisted carapace with the helmet and the tail spine deviating from the body axis into opposing directions, resulting in a complete abolishment of bilateral symmetry. The twisted morphotype should considerably interfere with the feeding apparatus of the predator, contributing to the effectiveness of the array of defensive traits in <i>D</i>. <i>barbata</i>. As such this study does not only describe a completely novel inducible defense in the genus <i>Daphnia</i> but also presents the first report of a free living Bilateria to flexibly respond to predation risk by abandoning bilateral symmetry.</p></div