Robby Stoks

Host–parasite ‘Red Queen’ dynamics archived in pond sediment

Antagonistic interactions between hosts and parasites are a key structuring force in natural populations, driving coevolution. However, direct empirical evidence of long-term host–parasite coevolution, in particular ‘Red Queen’ dynamics—in which antagonistic biotic interactions such as host–parasite interactions can lead to reciprocal evolutionary dynamics—is rare, and current data, although consistent with theories of antagonistic coevolution, do not reveal the temporal dynamics of the process. Dormant stages of both the water flea Daphnia and its microparasites are conserved in lake sediments, providing an archive of past gene pools. Here we use this fact to reconstruct rapid coevolutionary dynamics in a natural setting and show that the parasite rapidly adapts to its host over a period of only a few years. A coevolutionary model based on negative frequency-dependent selection, and designed to mimic essential aspects of our host–parasite system, corroborated these experimental results. In line with the idea of continuing host–parasite coevolution, temporal variation in parasite infectivity changed little over time. In contrast, from the moment the parasite was first found in the sediments, we observed a steady increase in virulence over time, associated with higher fitness of the parasite.

Life history plasticity in a damselfly : Effects of combined time and biotic constraints

Optimal values for life history traits are expected to depend upon environ- mental conditions during development and the period within which development is con- strained (e.g., biotic factors and time constraints, respectively). Theory predicts that life history responses to both biotic factors and time constraints may be both direct and be- haviorally mediated. Few experimental studies of life histories have considered the joint effects of biotic factors and time constraints, and fewer still have been able to disentangle direct from behaviorally mediated effects. We studied such interactions by manipulating the perceived time to the onset of winter, predation risk, and food resources level in larvae of the damselfly Lestes sponsa. In the first experiment (predation 3 time constraint), the presence of a predator caused an overall reduction in foraging activity, development rate, and mass at emergence. However, larvae that had less time available before the end of the season, increased foraging activity and development rate, while mass at emergence de- creased. These results suggest that the observed changes in life history characters were behaviorally mediated in the presence of predators. In contrast, life history responses of time-constrained larvae occurred independently of the behavioral changes and, therefore, were direct. In the second experiment (food level 3 time constraint) larvae under high food levels had a higher foraging activity, increased development rate, and higher growth rates, compared to low food-level treatments. Time-constrained larvae accelerated devel- opment and had a smaller mass at emergence at high food levels than larvae that were not time constrained. In contrast, and opposite to predictions, time-constrained larvae at low food levels had the slowest development rate and the largest mass at emergence. We suggest that larvae in the latter group were aiming to delay emergence to the next season (cohort splitting). Our results suggest that both behaviorally mediated and direct responses to biotic factors and time constraints are a feature of the life history of this damselfly.

FITNESS EFFECTS FROM EGG TO REPRODUCTION: BRIDGING THE LIFE HISTORY TRANSITION

Although complex life cycles are widespread, we know little about how constraints in the larval stage influence adult fitness. Most models assume a tight coupling of larval conditions and adult fitness through size and timing of the life history transition. However, there are few empirical tests of this assumption. We combined an experimental manipulation of larval environment with a subsequent study of adult fitness, measured as lifetime mating success. Individuals of the damselfly Lestes viridis were followed from the egg stage to adult reproduction and death. Under time constraints, emergence occurred earlier, but in late-hatched larvae, this did not result in a lower size. Under nutritional constraints, emergence occurred later, and size was reduced. Variation in survival to maturity was better explained by larval constraints than by emergence traits, whereas both larval constraints and emergence traits explained variation in lifetime mating success. Sexes reacted differently to larval constraints, and the coupling of larval constraints to adult fitness also was sex specific. Our results indicate that larval constraints do not necessarily carry over to adult fitness through size and timing of transition, and that carryover effects may be sex specific. This may explain the existence of hidden costs that become visible after maturation and may explain part of the unexplained variation in selection studies on adults.

PHYSIOLOGICAL COSTS OF COMPENSATORY GROWTH IN A DAMSELFLY

Little is known about physiological costs of rapid growth. We successfully generated compensatory growth to time stress and transient food stress in the damselfly Lestes viridis and studied the physiological correlates of the resulting reduced ability to cope with starvation. We found evidence for both mechanisms proposed to underlie the physiological trade-off: compensatory growth was associated with (1) a higher metabolic rate, as indicated by a higher oxygen consumption and a faster depletion of energy storage molecules (glycogen and triglycerides), and (2) a smaller investment in energy storage. The former may also explain why storage molecules after emergence were negatively affected by time stress and food stress, despite the successful compensation before emergence. These deferred physiological costs of rapid growth have the potential to couple larval stresses to adult fitness irrespective of age and size at emergence, and they may partly explain why many animals do not show their maximum achievable growth rate.

Evolutionary Ecology of Odonata: A Complex Life Cycle Perspective

Most insects have a complex life cycle with ecologically different larval and adult stages. We present an ontogenetic perspective to analyze and summarize the complex life cycle of Odonata within an evolutionary ecology framework. Morphological, physiological, and behavioral pathways that generate carry-over effects across the aquatic egg and larval stages and the terrestrial adult stage are identified. We also highlight several mechanisms that can decouple life stages including compensatory mechanisms at the larval and adult stages, stressful and stochastic events during metamorphosis, and stressful environmental conditions at the adult stage that may overrule effects of environmental conditions in the preceding stage. We consider the implications of these findings for the evolution, selection, and fitness of odonates; underline the role of the identified numerical and carry-over effects in shaping population and metapopulation dynamics and the community structure across habitat boundaries; and discuss implications for applied conservation issues.

TIME CONSTRAINTS MEDIATE PREDATOR-INDUCED PLASTICITY IN IMMUNE FUNCTION, CONDITION, AND LIFE HISTORY

The simultaneous presence of predators and a limited time for development imposes a conflict: accelerating growth under time constraints comes at the cost of higher predation risk mediated by increased foraging. The few studies that have addressed this tradeoff have dealt only with life history traits such as age and size at maturity. Physiological traits have largely been ignored in studies assessing the impact of environmental stressors, and it is largely unknown whether they respond independently of life history traits. Here, we studied the simultaneous effects of time constraints, i.e., as imposed by seasonality, and predation risk on immune defense, energy storage, and life history in lestid damselflies. As predicted by theory, larvae accelerated growth and development under time constraints while the opposite occurred under predation risk. The activity of phenoloxidase, an important component of insect immunity, and investment in fat storage were reduced both under time constraints and in the presence of predators. These reductions were smaller when time constraints and predation risk were combined. This indicates that predators can induce sublethal costs linked to both life history and physiology in their prey, and that time constraints can independently reduce the impact of predator-induced changes in life history and physiology.

Adaptive sex-specific life history plasticity to temperature and photoperiod in a damselfly

We investigated four predictions about how temperature, photoperiod and sex affect the life history plasticity and foraging activity of a damselfly. (i) As predicted, increased temperatures increased foraging activity and growth rates, but in contrast with the prediction, late photoperiod (high time stress) did not affect foraging activity and growth rate. (ii) Unexpectedly, the increase in growth rate at increasing temperatures was not larger under high time stress. (iii) As predicted, age and size at emergence decreased at higher temperatures and at the late photoperiod. Temperature‐induced life history shifts were direct or the result of behavioural growth mediation depending on the temperature range. Photoperiod‐induced life history shifts were direct. (iv) As predicted, males emerged before females but at a smaller size. The degree of sexual size dimorphism was influenced by the joint effects of temperature and photoperiod. We could only detect genetic variation in size plasticity to photoperiod. The match between the sex‐specific life history responses to temperature and photoperiod and predictions by relevant optimality models suggests adaptive life history plasticity to these variables.

Simultaneous Quaternary Radiations of Three Damselfly Clades across the Holarctic

If climate change during the Quaternary shaped the macroevolutionary dynamics of a taxon, we expect to see three features in its history: elevated speciation or extinction rates should date to this time, more northerly distributed clades should show greater discontinuities in these rates, and similar signatures of those effects should be evident in the phylogenetic and phylodemographic histories of multiple clades. In accordance with the role of glacial cycles, speciation rates increased in the Holarctic Enallagma damselflies during the Quaternary, with a 4.25× greater increase in a more northerly distributed clade as compared with a more southern clade. Finer‐scale phylogenetic analyses of three radiating clades within the northern clade show similar, complex recent histories over the past 250,000 years to produce 17 Nearctic and four Palearctic extant species. All three are marked by nearly synchronous deep splits that date to approximately 250,000 years ago, resulting in speciation in two. This was soon followed by significant demographic expansions in at least two of the three clades. In two, these expansions seem to have preceded the radiations that have given rise to most of the current biodiversity. Each also produced species at the periphery of the clade’s range. In spite of clear genetic support for reproductive isolation among almost all species, mtDNA signals of past asymmetric hybridization between species in different clades also suggest a role for the evolution of mate choice in generating reproductive isolation as species recolonized the landscape following deglaciation. These analyses suggest that recent climate fluctuations resulted in radiations driven by similar combinations of speciation processes acting in different lineages.

Evolutionary and plastic responses of freshwater invertebrates to climate change: realized patterns and future potential.

We integrated the evidence for evolutionary and plastic trait changes in situ in response to climate change in freshwater invertebrates (aquatic insects and zooplankton). The synthesis on the trait changes in response to the expected reductions in hydroperiod and increases in salinity indicated little evidence for adaptive, plastic, and genetic trait changes and for local adaptation. With respect to responses to temperature, there are many studies on temporal trait changes in phenology and body size in the wild that are believed to be driven by temperature increases, but there is a general lack of rigorous demonstration whether these trait changes are genetically based, adaptive, and causally driven by climate change. Current proof for genetic trait changes under climate change in freshwater invertebrates stems from a limited set of common garden experiments replicated in time. Experimental thermal evolution experiments and common garden warming experiments associated with space‐for‐time substitutions along latitudinal gradients indicate that besides genetic changes, also phenotypic plasticity and evolution of plasticity are likely to contribute to the observed phenotypic changes under climate change in aquatic invertebrates. Apart from plastic and genetic thermal adjustments, also genetic photoperiod adjustments are widespread and may even dominate the observed phenological shifts.

Coping with predator stress: interclonal differences in induction of heat‐shock proteins in the water flea Daphnia magna

Although predation is a strong selection pressure, little is known about the molecular mechanisms to cope with predator stress. This is crucial to understanding of the mechanisms and constraints involved in the evolution of antipredator traits. We quantified the expression of heat‐shock protein 60 (Hsp60), a potential marker for predator stress, in four clones of the water flea Daphnia magna, when exposed to fish kairomones. Expression of Hsp60 induction increased after 6 h and returned to base levels after 24 h of predator stress. This suggests that it is a costly transient mechanism to temporarily cope with novel predator stress, before other defences are induced. We found genetic variation in the fixed levels and in the fish‐induced levels of Hsp60, which seemed to be linked to each clones history of fish predation. Our data suggest that Hsp60 can be considered part of a multiple‐trait antipredator defence strategy of Daphnia clones to cope with predator stress.