Carita Lindstedt

THERMOREGULATION CONSTRAINS EFFECTIVE WARNING SIGNAL EXPRESSION

Evolution of conspicuous signals may be constrained if animal coloration has nonsignaling as well as signaling functions. In aposematic wood tiger moth (Parasemia plantaginis) larvae, the size of a warning signal (orange patch on black body) varies phenotypically and genetically. Although a large warning signal is favored as an antipredator defense, we hypothesized that thermoregulation may constrain the signal size in colder habitats. To test this hypothesis, we conducted a factorial rearing experiment with two selection lines for larval coloration (small and large signal) and with two temperature manipulations (high and low temperature environment). Temperature constrained the size and brightness of the warning signal. Larvae with a small signal had an advantage in the colder environment, which was demonstrated by a faster development time and growth rate in the low temperature treatment, compared to larvae with a large signal. Interestingly, the larvae with a small signal were found more often on the plant than the ones with a large signal, suggesting higher basking activity of the melanic (small signal) individuals in the low temperature. We conclude that the expression of aposematic display is not only defined by its efficacy against predators; variation in temperature may constrain evolution of a conspicuous warning signal and maintain variation in it.

Trade-off between warning signal efficacy and mating success in the wood tiger moth

The coloration of species can have multiple functions, such as predator avoidance and sexual signalling, that directly affect fitness. As selection should favour traits that positively affect fitness, the genes underlying the trait should reach fixation, thereby preventing the evolution of polymorphisms. This is particularly true for aposematic species that rely on coloration as a warning signal to advertise their unprofitability to predators. Nonetheless, there are numerous examples of aposematic species showing remarkable colour polymorphisms. We examined whether colour polymorphism in the wood tiger moth is maintained by trade-offs between different functions of coloration. In Finland, males of this species have two distinct colour morphs: white and yellow. The efficacy of the warning signal of these morphs was tested by offering them to blue tits in the laboratory. Birds hesitated significantly longer to attack yellow than white males. In a field experiment, the survival of the yellow males was also higher than white males. However, mating experiments in the laboratory revealed that yellow males had lower mating success than white males. Our results offer an explanation for the maintenance of polymorphism via trade-off between survival selection and mating success.

Changes in predator community structure shifts the efficacy of two warning signals in Arctiid moths

Polymorphism in warning coloration is puzzling because positive frequency-dependent selection by predators is expected to promote monomorphic warning signals in defended prey. We studied predation on the warning-coloured wood tiger moth (Parasemia plantaginis) by using artificial prey resembling white and yellow male colour morphs in five separate populations with different naturally occurring morph frequencies. We tested whether predation favours one of the colour morphs over the other and whether that is influenced either by local, natural colour morph frequencies or predator community composition. We found that yellow specimens were attacked less than white ones regardless of the local frequency of the morphs indicating frequency-independent selection, but predation did depend on predator community composition: yellows suffered less attacks when Paridae were abundant, whereas whites suffered less attacks when Prunellidae were abundant. Our results suggest that spatial heterogeneity in predator community composition can generate a geographical mosaic of selection facilitating the evolution of polymorphic warning signals. This is the first time this mechanism gains experimental support. Altogether, this study sheds light on the evolution of adaptive coloration in heterogeneous environments.

Predation on Multiple Trophic Levels Shapes the Evolution of Pathogen Virulence

The pathogen virulence is traditionally thought to co-evolve as a result of reciprocal selection with its host organism. In natural communities, pathogens and hosts are typically embedded within a web of interactions with other species, which could affect indirectly the pathogen virulence and host immunity through trade-offs. Here we show that selection by predation can affect both pathogen virulence and host immune defence. Exposing opportunistic bacterial pathogen Serratia marcescens to predation by protozoan Tetrahymena thermophila decreased its virulence when measured as host moth Parasemia plantaginis survival. This was probably because the bacterial anti-predatory traits were traded off with bacterial virulence factors, such as motility or resource use efficiency. However, the host survival depended also on its allocation to warning signal that is used against avian predation. When infected with most virulent ancestral bacterial strain, host larvae with a small warning signal survived better than those with an effective large signal. This suggests that larval immune defence could be traded off with effective defence against bird predators. However, the signal size had no effect on larval survival when less virulent control or evolved strains were used for infection suggesting that anti-predatory defence against avian predators, might be less constrained when the invading pathogen is rather low in virulence. Our results demonstrate that predation can be important indirect driver of the evolution of both pathogen virulence and host immunity in communities with multiple species interactions. Thus, the pathogen virulence should be viewed as a result of both past evolutionary history, and current ecological interactions.

Hairiness and warning colours as components of antipredator defence: additive or interactive benefits?

To deter predator attack, aposematic prey species advertise their unprofitability with one or more conspicuous warning signals that, in turn, enhance the avoidance learning of predators. We studied the costs and benefits of multicomponent signalling in Parasemia plantaginis moths. The hairy moth larvae have an orange patch on their otherwise black bodies. The patch varies phenotypically and genetically in size. We studied whether the detection risk associated with patch size varied against two backgrounds (green or brown) with two different predators: naive chicks, Gallus gallus domesticus, and experienced great tits, Parus major. We also evaluated the signal value of different defence traits within a multicomponent signal by testing which combination of two traits, hairiness and the presence or size of the orange patch, most affected the avoidance learning rate of predators. Larvae with a large orange patch were at greater risk of detection by birds against both backgrounds. This higher detection risk was traded-off with enhanced avoidance learning rate. The orange patch had a higher signal value for the predators than did hairiness, which only slightly increased the survival of totally black or small-patched larvae but did not affect the defence of larvae with a large orange patch. Multicomponent defences are therefore not necessarily additive and variation in the warning coloration of aposematic animals may be partly explained by variation in the relative benefits of different components of a warning signal to different predators.

Diet quality affects warning coloration indirectly: excretion costs in a generalist herbivore.

Aposematic herbivores are under selection pressure from their host plants and predators. Although many aposematic herbivores exploit plant toxins in their own secondary defense, dealing with these harmful compounds might underlay costs. We studied whether the allocation of energy to detoxification and/or sequestration of host plant defense chemicals trades off with warning signal expression. We used a generalist aposematic herbivore Parasemia plantaginis (Arctiidae), whose adults and larvae show extensive phenotypic and genetic variation in coloration. We reared larvae from selection lines for small and large larval warning signals on Plantago lanceolata with either low or high concentration of iridoid glycosides (IGs). Larvae disposed of IGs effectively; their body IG content was low irrespective of their diet. Detoxification was costly as individuals reared on the high IG diet produced fewer offspring. The IG concentration of the diet did not affect larval coloration (no trade‐off) but the wings of females were lighter orange (vs. dark red) when reared on the high IG diet. Thus, the difference in plant secondary chemicals did not induce variation in the chemical defense efficacy of aposematic individuals but caused variation in reproductive output and warning signals of females.

High Temperature and Bacteriophages Can Indirectly Select for Bacterial Pathogenicity in Environmental Reservoirs

The coincidental evolution hypothesis predicts that traits connected to bacterial pathogenicity could be indirectly selected outside the host as a correlated response to abiotic environmental conditions or different biotic species interactions. To investigate this, an opportunistic bacterial pathogen, Serratia marcescens, was cultured in the absence and presence of the lytic bacteriophage PPV (Podoviridae) at 25°C and 37°C for four weeks (N = 5). At the end, we measured changes in bacterial phage-resistance and potential virulence traits, and determined the pathogenicity of all bacterial selection lines in the Parasemia plantaginis insect model in vivo. Selection at 37°C increased bacterial motility and pathogenicity but only in the absence of phages. Exposure to phages increased the phage-resistance of bacteria, and this was costly in terms of decreased maximum population size in the absence of phages. However, this small-magnitude growth cost was not greater with bacteria that had evolved in high temperature regime, and no trade-off was found between phage-resistance and growth rate. As a result, phages constrained the evolution of a temperature-mediated increase in bacterial pathogenicity presumably by preferably infecting the highly motile and virulent bacteria. In more general perspective, our results suggest that the traits connected to bacterial pathogenicity could be indirectly selected as a correlated response by abiotic and biotic factors in environmental reservoirs.

Disengtangling the evolution of weak warning signals: high detection risk and low production costs of chemical defences in gregarious pine sawfly larvae

Evolution of costly secondary defences for a cryptic prey is puzzling, if the prey is already well protected by camouflage. However, if the chemical defence is not sufficient to deter all predators, selection can favour low signal intensity in defended prey. Alternatively, if the costs of chemical defence are low or cost-free, chemical defences can be expected to evolve also for non-signalling prey, particularly if conspicuous signalling is costly. We tested these assumptions with pine sawfly larvae (Neodiprion sertifer and Diprion pini) that are cryptically coloured and chemically defended with resin acids sequestered from their host plant (Pinus sp.). Larvae feed in large aggregations, which we hypothesise could function as a signal of unprofitability. Our results show that even though the birds found N. sertifer larvae unprofitable in the controlled laboratory assays, they continued attacking and consuming them in the wild. When we tested the signal value of aggregation we found that a large group size did not offer protection for a defended larva: the survival was higher in groups of 10 individuals compared to groups of 50, suggesting increased detectability costs for individuals in larger groups. Finally, we tested how costly the production and maintenance of a chemical defence is for D. pini larvae by manipulating the resin acid content of the diet. We did not find any life history or immunological costs of the chemical defence for the larvae. In contrast, pupal weights were higher on the high resin diet than on the low resin diet. Also, larvae were able to produce higher amounts of defence fluids on the high diet than on the low diet. Thus, our result suggests high detectability costs and low production costs of defences could explain why some unprofitable species have not evolved conspicuous signals.

Diet Quality Can Play a Critical Role in Defense Efficacy against Parasitoids and Pathogens in the Glanville Fritillary (Melitaea cinxia)

Numerous herbivorous insect species sequester noxious chemicals from host plants that effectively defend against predators, and against parasitoids and pathogens. Sequestration of these chemicals may be expensive and involve a trade off with other fitness traits. Here, we tested this hypothesis. We reared Glanville fritillary butterfly (Melitaea cinxia L.) larvae on plant diets containing low- and high-levels of iridoid glycosides (IGs) (mainly aucubin and catalpol) and tested: 1) whether IGs affect the herbivore’s defense against parasitoids (measured as encapsulation rate) and bacterial pathogens (measured as herbivore survival); 2) whether parasitoid and bacterial defenses interact; and 3) whether sequestration of the plant’s defense chemicals incurs any life history costs. Encapsulation rates were stronger when there were higher percentages of catalpol in the diet. Implanted individuals had greater amounts of IGs in their bodies as adults. This suggests that parasitized individuals may sequester more IGs, increase their feeding rate after parasitism, or that there is a trade off between detoxification efficiency and encapsulation rate. Larval survival after bacterial infection was influenced by diet, but probably not by diet IG content, as changes in survival did not correlate linearly with the levels of IGs in the diet. However, M. cinxia larvae with good encapsulation abilities were better defended against bacteria. We did not find any life history costs of diet IG concentration for larvae. These results suggest that the sequestering of plant defense chemicals can help herbivorous insects to defend against parasitoids.

The evolutionary ecology of deception

Through dishonest signals or actions, individuals often misinform others to their own benefit. We review recent literature to explore the evolutionary and ecological conditions for deception to be more likely to evolve and be maintained. We identify four conditions: (1) high misinformation potential through perceptual constraints of perceiver; (2) costs and benefits of responding to deception; (3) asymmetric power relationships between individuals and (4) exploitation of common goods. We discuss behavioural and physiological mechanisms that form a deception continuum from secrecy to overt signals. Deceptive tactics usually succeed by being rare and are often evolving under co‐evolutionary arms races, sometimes leading to the evolution of polymorphism. The degree of deception can also vary depending on the environmental conditions. Finally, we suggest a conceptual framework for studying deception and highlight important questions for future studies.