Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi

1. The exotic cladoceran Daphnia lumholtzi has recently invaded freshwater systems throughout the United States. Daphnia lumholtzi possesses extravagant head spines that are longer than those found on any other North American Daphnia. These spines are effective at reducing predation from many of the predators that are native to newly invaded habitats; however, they are plastic both in nature and in laboratory cultures. The purpose of this experiment was to better understand what environmental cues induce and maintain these effective predator‐deterrent spines. We conducted life‐table experiments on individual D. lumholtzi grown in water conditioned with an invertebrate insect predator, Chaoborus punctipennis, and water conditioned with a vertebrate fish predator, Lepomis macrochirus. 2. Daphnia lumholtzi exhibited morphological plasticity in response to kairomones released by both predators. However, direct exposure to predator kairomones during postembryonic development did not induce long spines in D. lumholtzi. In contrast, neonates produced from individuals exposed to Lepomis kairomones had significantly longer head and tail spines than neonates produced from control and Chaoborus individuals. These results suggest that there may be a maternal, or pre‐embryonic, effect of kairomone exposure on spine development in D. lumholtzi. 3. Independent of these morphological shifts, D. lumholtzi also exhibited plasticity in life history characteristics in response to predator kairomones. For example, D. lumholtzi exhibited delayed reproduction in response to Chaoborus kairomones, and significantly more individuals produced resting eggs, or ephippia, in the presence of Lepomis kairomones.     

Juvenile exposure to predator cues induces a larger egg size in fish

When females anticipate a hazardous environment for their offspring, they can increase offspring survival by producing larger young. Early environmental experience determines egg size in different animal taxa. We predicted that a higher perceived predation risk by juveniles would cause an increase in the sizes of eggs that they produce as adults. To test this, we exposed juveniles of the mouthbrooding cichlid Eretmodus cyanostictus in a split-brood experiment either to cues of a natural predator or to a control situation. After maturation, females that had been confronted with predators produced heavier eggs, whereas clutch size itself was not affected by the treatment. This effect cannot be explained by a differential female body size because the predator treatment did not influence growth trajectories. The observed increase of egg mass is likely to be adaptive, as heavier eggs gave rise to larger young and in fish, juvenile predation risk drops sharply with increasing body size. This study provides the first evidence that predator cues perceived by females early in life positively affect egg mass, suggesting that these cues allow her to predict the predation risk for her offspring.     

Embryological aspects of inducible morphological defenses in Daphnia

Many cases of predator-induced morphological plasticity in daphnids are well studied examples of inducible defenses. However, little is known about the early development of these sometimes conspicuous traits. We compared for the first time in five different Daphnia species the embryonic development of predator-induced and noninduced animals using scanning electron microscopy (SEM). We observed significant morphological changes in the last embryonic stage in helmet formation in Daphnia cucullata and in neck-pedestal development in Daphnia pulex. In contrast, no morphological changes could be found during embryogenesis between induced and noninduced Daphnia lumholtzi, D. longicephala, and D. ambigua. Strategies for initiating the defensive traits differ among Daphnia species because of trade-offs between environmental requirements and developmental constraints. Some general features of Daphnia embryonic development are described using SEM. All Daphnia embryos have to shed at least three different membranes before leaving the brood pouch of the mother. After the embryos shed the third membrane, chemosensillae that are likely able to detect predator-released chemicals are exposed to the olfactory environment.     

Food level reaction norms in size-selected milkweed bugs (Oncopeltus fasciatus)

Abstract. 1. The hypothesis that the small size of nonmigratory milkweed bugs from Puerto Rico (relative to large migratory bugs from Iowa) might be an adaptation to low food levels was tested with bugs selected for large and small size as the consequence of positive genetic correlation between body size and wing length. The test involved examining reaction norms of life history traits to different food levels.
2. When nymphs were reared on 3 milkweed seeds per nymph from hatch to adult eclosion, large bugs were adversely affected with only 50% and 60% in each of two replicates reaching adulthood. Control (unselected) and small bugs, however, were unaffected at this food level. None of the lines was affected at levels of 6 and 12 seeds per nymph.
3. When adults were reared from eclosion on 12, 18 or 24 milkweed seeds per bug, large bugs were adversely affected relative to control and small bugs at all three food levels. At each food level fewer large bugs produced eggs than either small or control bugs which did not differ.
4. The evidence from the food level reaction norms suggests that larger bugs will be selected against during periods of food shortage of the sort likely to occur in Puerto Rico.     

The evolution of life histories in spatially heterogeneous environments: Optimal reaction norms revisited

Summary Natural populations live in heterogeneous environments, where habitat variation drives the evolution of phenotypic plasticity. The key feature of population structure addressed in this paper is the net flow of individuals from source (good) to sink (poor) habitats. These movements make it necessary to calculate fitness across the full range of habitats encountered by the population, rather than independently for each habitat. As a consequence, the optimal phenotype in a given habitat not only depends on conditions there but is linked to the performance of individuals in other habitats. We generalize the Euler-Lotka equation to define fitness in a spatially heterogeneous environment in which individuals disperse among habitats as newborn and then stay in a given habitat for life. In this case, maximizing fitness (the rate of increase over all habitats) is equivalent to maximizing the reproductive value of newborn in each habitat but not to maximizing the rate of increase that would result if individuals in each habitat were an isolated population. The new equation can be used to find optimal reaction norms for life history traits, and examples are calculated for age at maturity and clutch size. In contrast to previous results, the optimal reaction norm differs from the line connecting local adaptations of isolated populations each living in only one habitat. Selection pressure is higher in good and frequent habitats than in poor and rare ones. A formula for the relative importance of these two factors allows predictions of the habitat in which the genetic variance about the optimal reaction norm should be smallest.     

Plasticity in probabilistic reaction norms for maturation in a salmonid fish

The relationship between body size and the probability of maturing, often referred to as the probabilistic maturation reaction norm (PMRN), has been increasingly used to infer genetic variation in maturation schedule. Despite this trend, few studies have directly evaluated plasticity in the PMRN. A transplant experiment using white-spotted charr demonstrated that the PMRN for precocious males exhibited plasticity. A smaller threshold size at maturity occurred in charr inhabiting narrow streams where more refuges are probably available for small charr, which in turn might enhance the reproductive success of sneaker precocious males. Our findings suggested that plastic effects should clearly be included in investigations of variation in PMRNs.     

Migrating Daphnia have a memory for fish kairomones

Kairomones from juvenile perch (Perca fluviatilis) enhance phototactic descent of Daphnia to the hypolimnion of lakes following upon light intensity increases at dawn. Kairomones are not present in the hypolimnion and ascent in the evening might be insufficient for the animals to reach the epilimnion again. The hypothesis that sensitization is maintained for some time in the absence of fish exudates was tested. Experiments showed that sensitization was indeed maintained for 5–6 days. Thus a kind of “memory”; for fish kairomones exists, resulting in an enhanced ascent from a fishless hypolimnion at sunset.     

Larval fish-induced phenotypic plasticity of coexisting Daphnia: an enclosure experiment

1. The indirect effects of predators on lower trophic levels have been studied without much attention to phenotypically plastic traits of key food web components. Phenotypic plasticity among species creates phenotypic diversity over a changing environmental landscape. 2. We measured the indirect effects of planktivorous larval walleye (Stizostedion vitreum) on phytoplankton biomass through their effects on the dominant herbivore species, Daphnia pulicaria and D. mendotae. 3. Fish had no effect on phytoplankton biomass or overall Daphnia density. We observed a compensatory response to predation by functionally comparable species within a trophic level in the form of shifting dominance and coexistence of Daphnia species. We hypothesized that this phenotypically plastic response to predation decoupled a potential trophic cascade in this freshwater pelagic system. Daphnia pulicaria density decreased over time with fish predation, but D. mendotae density increased over time with fish predation. 4. Phenotypically plastic life history trait shifts and reproductive rates differed between species in fishless and fish enclosures, accounting for population trends. Daphnia pulicaria were also proportionally higher in walleye larvae stomachs than in the enclosures, indicating that walleye preferred to feed on D. pulcaria over D. mendotae. The resultant shift in dominance may partially explain the overall benign effect of fish on grazers and supports the hypothesis that trophic level diversity can decouple a trophic cascade.     

Parasite survey of a Daphnia hybrid complex: host-specificity and environment determine infection

1. Hybridization between species is a common phenomenon in plants and animals. If parasite prevalence differs for hybrids and parental species (i.e. taxa) there may be considerable consequences for relative hybrid fitness. Some studies have investigated hybrid complexes for infection, and complex-specific differences in parasite prevalence have been detected. 2. Based on the results of a field study on a hybridizing Daphnia population from a single lake, it has been hypothesized that permanently over- or under-infected hybrids do not exist. The observed field-patterns can only be temporal because taxa, in addition to single genotypes, might be the subject of parasite driven host frequency-dependent selection. Thus, parasites will track any common taxon within a hybrid complex. 3. In the present study, hybridizing Daphnia populations from 43 lakes were screened for parasite infections to obtain indirect evidence for coevolutionary cycles. It was hypothesized that, due to time lags between the evolution of resistance in host populations and the evolution of the parasite towards tracking of a common host taxon, the same Daphnia taxon will be over-infected in some lakes, while being under-infected in others. 4. Two of the four parasite species were specialists: their prevalence differed among coexisting Daphnia taxa. The varying infection patterns detected across spatially segregated hybridizing Daphnia populations are consistent with theoretical predictions for coevolutionary cycles. Thus the infection patterns, as observed under natural conditions, are temporal and unstable. 5. Additionally, the spatial distribution of the four parasite species was analysed with respect to habitat differences. The results show that the presence of a particular parasite on a host taxon was determined not only by the host-specificity of the parasite, but also by host-habitat relations.     

The evolution of reaction norms: simple models for age and size at maturity

This paper presents a simple model for the evolution of reaction norms for age and size at maturity that predicts reaction norms with a variety of shapes. Using realistic parameter values the model predicts reaction norms close to those observed in Drosophila. The major assumptions of the model are: 1) that net reproductive rate is maximized, 2) that growth is determinate, and 3) that mortality rates are independent of age and size at maturity. If, additionally, juvenile mortality is uncorrelated with a growth coefficient, k, the model predicts that selection favors maturation later at a smaller size when k is reduced by environmental factors and that decreased juvenile mortality leads to delayed maturity. These two predictions conform with those found by previous models using other measures of fitness. Correlations between k and juvenile mortality can change the shape of the predicted reaction norm. Depending on the precise form of the correlation, the model can predict done- or bowl-shaped reaction norms and can predict delayed or earlier maturity as k decreases. These shapes are qualitatively different from those predicted by previous models that used different fitness measures. Systematic estimates of the parameter values for this and for related models are required to determine the appropriate fitness measure for models of reaction norms.     

Sex-specific reaction norms to intraspecific larval competition in the mosquito Aedes aegypti

As the relationship between a given life‐history trait and fitness is not necessarily the same for the two sexes, an ‘intersexual ontogenetic conflict’ may arise. We analysed the phenotypic reaction to intraspecific larval competition of the mosquito, Aedes aegypti, asking: (i) Do both sexes pay the cost of competition with the same life‐history traits and are they equal competitors? (ii) Is there a specific cost of competition beyond sharing food resources? We found that competition incurs a specific cost that was expressed differently by the two sexes. Indeed, each sex maintained the more important life‐history trait(s) for their fitness (developmental time for males and body weight and size for females) at the expense of other traits, thus minimizing the effects of competition on their fitness. The competition exerted by females was estimated as being more intense, probably linked with the greater importance of body size for their fitness.     

Gene regulation,quantitative genetics and the evolution of reaction norms

Summary The ideas of phenotypic plasticity and of reaction norm are gaining prominence as important components of theories of phenotypic evolution. Our understanding of the role of phenotypic plasticity as an adaptation of organisms to variable environments will depend on (1) the form(s) of genetic and developmental control exerted on the shape of the reaction norm and (2) the nature of the constraints on the possible evolutionary trajectories in multiple environments. In this paper we identify two categories of genetic control of plasticity: allelic sensitivity and gene regulation. These correspond generally to two classes of response by the developmental system to environmental change: phenotypic modulation, in which plastic responses are a continuous and proportional function of environmental stimuli and developmental conversion, where responses tend to be not simply proportional to the stimuli. We propose that control of plasticity by regulatory actions has distinct advantages over simple allelic sensitivity: stability of phenotypic expression, capacity for anticipatory response and relaxation of constraints due to genetic correlations. We cite examples of the extensive molecular evidence for the existence of environmentally-cued gene regulation leading to developmental conversion. The results of quantitative genetic investigations on the genetics and evolution of plasticity, as well as the limits of current approaches are discussed. We suggest that evolution of reaction norms would be affected by the ecological context (i.e. spatial versus temporal variation, hard versus soft selection, and fine versus coarse environmental grain). We conclude by discussing some empirical approaches to address fundamental questions about plasticity evolution.     

Fitness and sexual response to population density in Daphnia pulex

1. The switch between asexual and sexual reproduction is an important fitness component in cyclically parthenogenetic populations as it is the key to persistence in unstable habitats and because it influences population genetic characteristics such as linkage disequilibrium and population genetic structure.
2. Genetic variation for sexual and asexual reproductive rate ( R _C) was examined, under varying population density, in Daphnia pulex sampled from a rockpool system and two other distinct European localities.
3. Density affected the switch to sexual behaviour, as found in other studies and reduced R _c. Production of males was not correlated with sexual reproduction, promoting outcrossing.
4. Genetic variation was found for the response to density, both within and between populations. There was substantial variation within the rockpools despite their demographic instability, indicating rapid recovery of life-history variation or maintenance during bottlenecks.     

Temperature reaction norms of Daphnia magna: the effect of food concentration

1. The effects of temperature and food concentration on the fitness of Daphnia magna were tested in a 4×4 factorial flow-through design. Food ranged from 0.1 to 1.0 mg C L⁻¹ and temperature ranged from 15 to 30 °C. 2. The juvenile growth rate ( g _j) was used to construct reaction norms for temperature at varying food concentrations. Two clones isolated from the same pond at different seasons did not differ with respect to their temperature responses. Reaction norms had the shape of an optimum curve with highest values around 20 °C. There was a significant temperature–food interaction as the temperature response was most pronounced when the food was not limiting. 3. Differences in fitness were a consequence of different responses of physiological parameters to food and temperature. Age and size at first reproduction, as well as egg numbers, decreased with increasing temperature and decreasing food concentration. 4. As the temperature effect was strongest at the highest food concentrations, it can be concluded that environmental warming may affect D. magna more through a temperature rise earlier in spring rather than in summer.     

Translating environmental gradients into discontinuous reaction norms via hormone signalling in a polyphenic butterfly

Polyphenisms—the expression of discrete phenotypic morphs in response to environmental variation—are examples of phenotypic plasticity that may potentially be adaptive in the face of predictable environmental heterogeneity. In the butterfly Bicyclus anynana, we examine the hormonal regulation of phenotypic plasticity that involves divergent developmental trajectories into distinct adult morphs for a suite of traits as an adaptation to contrasting seasonal environments. This polyphenism is induced by temperature during development and mediated by ecdysteroid hormones. We reared larvae at separate temperatures spanning the natural range of seasonal environments and measured reaction norms for ecdysteroids, juvenile hormones (JHs) and adult fitness traits. Timing of peak ecdysteroid, but not JH titres, showed a binary response to the linear temperature gradient. Several adult traits (e.g. relative abdomen mass) responded in a similar, dimorphic manner, while others (e.g. wing pattern) showed a linear response. This study demonstrates that hormone dynamics can translate a linear environmental gradient into a discrete signal and, thus, that polyphenic differences between adult morphs can already be programmed at the stage of hormone signalling during development. The range of phenotypic responses observed within the suite of traits indicates both shared regulation and independent, trait-specific sensitivity to the hormone signal.     

The selective advantage of reaction norms for environmental tolerance

A tolerance curve defines the dependence of a genotype's fitness on the state of an environmental gradient. It can be characterized by a mode (the genotype's optimal environment) and a width (the breadth of adaptation). It seems possible that one or both of these characters can be modified in an adaptive manner, at least partially, during development. Thus, we extend the theory of environmental tolerance to include reaction norms for the mode and the width of the tolerance curve. We demonstrate that the selective value of such reaction norms increases with increasing spatial heterogeneity and between-generation temporal variation in the environment and with decreasing within-generation temporal variation. Assuming that the maintenance of a high breadth of adaptation is costly, reaction, norms are shown to induce correlated selection for a reduction in this character. Nevertheless, regardless of the magnitude of the reaction norm, there is a nearly one to one relationship between the optimal breadth of adaptation and the within-generation temporal variation perceived by the organism. This suggests that empirical estimates of the breadth of adaptation may provide a useful index of this type of environmental variation from the organism's point of view.     

Reaction norms of life history traits in response to zinc in Thlaspi caerulescens from metalliferous and nonmetalliferous sites

* We examined phenotypic plasticity of fitness components in response to zinc (Zn) in the Zn hyperaccumulator, Thlaspi caerulescens. * Two populations from Zn-enriched soils (M) and two populations from normal soils (NM) were grown in pots at three Zn concentrations (0, 1000 and 8000 mg kg(-1) Zn), for an entire life cycle. Growth, Zn accumulation and fitness components were assessed. * Based on vegetative growth, M and NM populations had similar Zn tolerance at 1000 mg kg(-1) Zn. However, reproductive output was markedly decreased in NM at 1000 and 8000 mg kg(-1) Zn. In M populations, Zn did not affect fitness. However, low Zn status enhanced reproductive output in year 1 compared with year 2 and decreased survival after the first flowering season. * M populations are able to achieve equal fitness across a broad range of Zn concentrations in soil by different combinations of fecundity and longevity. No cost of higher tolerance was demonstrated in M populations. Reproductive traits appeared to be a more sensitive indicator of tolerance than vegetative growth.