0000000000073187
AUTHOR
Carita Lindstedt
Evolutionary constraints of warning signals: A genetic trade-off between the efficacy of larval and adult warning coloration can maintain variation in signal expression
To predict evolutionary responses of warning signals under selection, we need to determine the inheritance pattern of the signals, and how they are genetically correlated with other traits contributing to fitness. Furthermore, protective coloration often undergoes remarkable changes within an individual's lifecycle, requiring us to quantify the genetic constraints of adaptive coloration across all the relevant life stages. Based on a 12 generation pedigree with > 11,000 individuals of the wood tiger moth (Arctia plantaginis), we show that high primary defense as a larva (large warning signal) results in weaker defenses as adult (less efficient warning color), due to the negative genetic cor…
Defense against predators incurs high reproductive costs for the aposematic moth Arctia plantaginis
Abstract To understand how variation in warning displays evolves and is maintained, we need to understand not only how perceivers of these traits select color and toxicity but also the sources of the genetic and phenotypic variation exposed to selection by them. We studied these aspects in the wood tiger moth Arctia plantaginis, which has two locally co-occurring male color morphs in Europe: yellow and white. When threatened, both morphs produce defensive secretions from their abdomen and from thoracic glands. Abdominal fluid has shown to be more important against invertebrate predators than avian predators, and the defensive secretion of the yellow morph is more effective against ants. Her…
Gray plumage color is more cryptic than brown in snowy landscapes in a resident color polymorphic bird
Abstract Camouflage may promote fitness of given phenotypes in different environments. The tawny owl (Strix aluco) is a color polymorphic species with a gray and brown morph resident in the Western Palearctic. A strong selection pressure against the brown morph during snowy and cold winters has been documented earlier, but the selection mechanisms remain unresolved. Here, we hypothesize that selection favors the gray morph because it is better camouflaged against predators and mobbers in snowy conditions compared to the brown one. We conducted an online citizen science experiment where volunteers were asked to locate a gray or a brown tawny owl specimen from pictures taken in snowy and snow…
Evolutionary constraints of warning signals : a genetic trade-off between the efficacy of larval and adult warning coloration can maintain variation in signal expression
To predict evolutionary responses of warning signals under selection, we need to determine the inheritance pattern of the signals, and how they are genetically correlated with other traits contributing to fitness. Furthermore, protective coloration often undergoes remarkable changes within an individual's lifecycle, requiring us to quantify the genetic constraints of adaptive coloration across all the relevant life stages. Based on a 12 generation pedigree with > 11,000 individuals of the wood tiger moth (Arctia plantaginis), we show that high primary defense as a larva (large warning signal) results in weaker defenses as adult (less efficient warning color), due to the negative genetic cor…
Variation in male fertility in a polymorphic moth, Parasemia plantaginis
The maintenance of multiple morphs in warning signals is enigmatic because directional selection through predator avoidance should lead to the rapid loss of such variation. Opposing natural and sexual selection is a good candidate driving the maintenance of multiple male morphs but it also includes another enigma: when warning signal efficiency differs between male morphs, why would females choose a phenotype with lower survival? We tested the hypothesis that indirect responses to selection on correlated characters through sexual selection may substantially shape the evolution of male coloration. If male phenotypes differ in their fertilization ability, female choice against the best surviv…
Do avian predators select for seasonal polyphenism in the European map butterfly Araschnia levana (Lepidoptera: Nymphalidae)?
Seasonal polyphenism in animal colour patterns indicates that temporal variation in selection pressures maintains phenotypic plasticity. Spring generation of the polyphenic European map butterfly Araschnia levana has an orange–black fritillary-like pattern whilst individuals of the summer generation are black with white bands across the wings. What selects for the colour difference is unknown. Because predation is a major selection pressure for insect coloration, we first tested whether map butterfly coloration could have a warning function (i.e. whether the butterflies are unpalatable to birds). In a following field experiment with butterfly dummies we tested whether the spring form is bet…
Antipredator strategies of pupae: how to avoid predation in an immobile life stage?
Antipredator strategies of the pupal stage in insects have received little attention in comparison to larval or adult stages. This is despite the fact that predation risk can be high during the pupal stage, making it a critical stage for subsequent fitness. The immobile pupae are not, however, defenceless; a wide range of antipredator strategies have evolved against invertebrate and vertebrate predators. The most common strategy seems to be ‘avoiding encounters with predators' by actively hiding in vegetation and soil or via cryptic coloration and masquerade. Pupae have also evolved behavioural and secondary defences such as defensive toxins, physical defences or deimatic movements and soun…
Parental care shapes evolution of aposematism and provides lifelong protection against predators
ABSTRACTSocial interactions within species can modulate the response to selection and determine the extent of evolutionary change. Yet relatively little work has determined whether the social environment can influence the evolution of traits that are selected by interactions with other species - a major source of natural selection. Here we show that the amount of parental care received as an offspring can influence the expression, and potential evolution, of warning displays deployed against predators in adulthood. In theory, warning displays by prey are selected by predators for uniformity and to reliably advertise the extent to which individuals are chemically defended. However, the corre…
Appearance before performance? : Nutritional constraints on life‐history traits, but not warning signal expression in aposematic moths
1.Trade‐offs have been shown to play an important role in the divergence of mating strategies and sexual ornamentation, but their importance in explaining warning signal diversity has received less attention. In aposematic organisms, allocation costs of producing the conspicuous warning signal pigmentation under nutritional stress could potentially trade‐off with life‐history traits and maintain variation in warning colouration. 2. We studied this with an aposematic herbivore Arctia plantaginis (Arctiidae), whose larvae and adults show extensive variation in aposematic colouration. In larvae, less melanic colouration (i.e. larger orange patterns) produces a more efficient warning signal aga…
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 br…
The evolution and ecology of multiple antipredator defences
Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such “defence portfolios” that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of speci…
The impact of life stage and pigment source on the evolution of novel warning signal traits
Our understanding of how novel warning color traits evolve in natural populations is largely based on studies of reproductive stages and organisms with endogenously produced pigmentation. In these systems, genetic drift is often required for novel alleles to overcome strong purifying selection stemming from frequency-dependent predation and positive assortative mating. Here, we integrate data from field surveys, predation experiments, population genomics, and phenotypic correlations to explain the origin and maintenance of geographic variation in a diet-based larval pigmentation trait in the redheaded pine sawfly (Neodiprion lecontei), a pine-feeding hymenopteran. Although our experiments c…
Sex ratio and sexual conflict in a collective action problem
AbstractThe maintenance of cooperation is difficult whenever collective action problems are vulnerable to freeriding (reaping the benefits without contributing to the maintenance of the good). We identify a novel factor that can make a system tolerate an extent of freeriding. If a population consists of discrete types with demographically distinct roles, such that the success of one type does not imply it can spread to replace other types in the population, then collective goods may persist in the presence of free-riders because they are necessarily kept in a minority role. Biased sex ratios (e.g. in haplodiploids) create conditions where individuals of one sex are a minority. We show that …
Ecological conditions alter cooperative behaviour and its costs in a chemically defended sawfly
The evolution of cooperation and social behaviour is often studied in isolation from the ecology of organisms. Yet, the selective environment under which individuals evolve is much more complex in nature, consisting of ecological and abiotic interactions in addition to social ones. Here, we measured the life-history costs of cooperative chemical defence in a gregarious social herbivore, Diprion pini pine sawfly larvae, and how these costs vary under different ecological conditions. We ran a rearing experiment where we manipulated diet (resin content) and attack intensity by repeatedly harassing larvae to produce a chemical defence. We show that forcing individuals to allocate more to coope…
Maintenance of variation in warning signals under opposing selection pressures
Kaikki eliöt ovat jotain kautta yhteydessä toisiin eliöihin erilaisten vuorovaikutussuhteiden kautta. Tyypillisesti vihollisiakaan ei ole vain yhtä, vaan useita erilaisia, joiden määrät ja tiheydet vaihtelevat luonnossa. Useisiin vastakkaisiin ja vaihteleviin valintapaineisiin on hankalaa sopeutua.Tilanne on haaste myös tutkijalle, sillä on vaikeampaa tutkia useampia valintapaineita samanaikaisesti kuin vain yhtä kerrallaan. Eläinten väritys antaa kuitenkin hyvän mahdollisuuden useiden samanaikaisten valintapaineiden tutkimiselle. Väritystä ja sen muuntelua on helppo havaita ja värityksellä on suuri merkitys eläimen hengissä selviytymisen kannalta.Carita Lindstedtin väitöskirjatutkimuksen l…
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 o…
Characterizing the pigment composition of a variable warning signal of Parasemia plantaginis larvae
Summary 1. Aposematic animals advertise their defences to predators via warning signals that often are bright colours combined with black patterns. Predation is assumed to select for large pattern elements and conspicuousness of warning signals because this enhances avoidance learning of predators. However, conspicuousness of the colour pattern can vary among individuals of aposematic species, suggesting that warning signal expression may be constrained by opposing selection pressures. If effective warning signals are costly to produce, variation in signal expression may be maintained via physiological trade-offs. To understand the costs of signalling that might underlay both physiological …
Direction and strength of selection by predators for the color of the aposematic wood tiger moth
Conventionally, predation is assumed to select for conspicuousness and uniformity of warning signals in aposematic (i.e., chemically defended and warning signaling) prey because this enhances predators' initial and learned avoidance. On the other hand, it has been suggested that both variation in the background where the signal is displayed as well as variation in predators' probability to attack defended prey may favor intermediate signals or relax selection for signal monomorphism. We studied the direction and strength of selection for the hind wing color (orange vs. red) of female Parasemia plantaginis moths. Birds found the moths aversive and avoided them by sight both in laboratory and…
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 concentratio…
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, m…
Genetic Basis of Body Color and Spotting Pattern in Redheaded Pine Sawfly Larvae (Neodiprion lecontei)
Abstract Pigmentation has emerged as a premier model for understanding the genetic basis of phenotypic evolution, and a growing catalog of color loci is starting to reveal biases in the mutations, genes, and genetic architectures underlying color variation in the wild. However, existing studies have sampled a limited subset of taxa, color traits, and developmental stages. To expand the existing sample of color loci, we performed QTL mapping analyses on two types of larval pigmentation traits that vary among populations of the redheaded pine sawfly (Neodiprion lecontei): carotenoid-based yellow body color and melanin-based spotting pattern. For both traits, our QTL models explained a substan…
Multimodal Aposematic Signals and Their Emerging Role in Mate Attraction
Chemically defended animals often display conspicuous color patterns that predators learn to associate with their unprofitability and subsequently avoid. Such animals (i.e., aposematic), deter predators by stimulating their visual and chemical sensory channels. Hence, aposematism is considered to be “multimodal.” The evolution of warning signals (and to a lesser degree their accompanying chemical defenses) is fundamentally linked to natural selection by predators. Lately, however, increasing evidence also points to a role of sexual selection shaping warning signal evolution. One of the species in which this has been shown is the wood tiger moth, Arctia plantaginis, which we here put forward…
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 trai…
Aposematism in the burying beetle? Dual function of anal fluid in parental care and chemical defence
Burying beetles (Nicrophorus vespilloides) bear distinctive and variable orange-black patterning on their elytra and produce an anal exudate from their abdomen when threatened. During breeding, the anal exudates contribute to the antimicrobial defence of the breeding resource. We investigated whether the anal exudates also provide a responsive chemical defence, which is advertised to potential avian predators by the beetle’s orange and black elytral markings. We found that that the orange-black elytral markings of the burying beetle are highly conspicuous for avian predators against range of backgrounds, by using computer simulations. Using bioassays with wood ants, we also showed that the …
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…
Costs and benefits of plant allelochemicals in herbivore diet in a multi enemy world
Sequestration of plant defensive chemicals by herbivorous insects is a way of defending themselves against their natural enemies. Such herbivores have repeatedly evolved bright colours to advertise their unpalatability to predators, i.e. they are aposematic. This often comes with a cost. In this study, we examined the costs and benefits of sequestration of iridoid glycosides (IGs) by the generalist aposematic herbivore, the wood tiger moth, Parasemia plantaginis. We also asked whether the defence against one enemy (a predator) is also effective against another (a parasitoid). We found that the larvae excrete most of the IGs and only small amounts are found in the larvae. Nevertheless, the a…
Effect of Willow TitPoecile montanusalarm calls on attack rates by Pygmy OwlsGlaucidium passerinum
One suggested anti-predator function of alarm calls is to deliver a message to a predator that it has been detected. Moreover, giving the alarm call could provide a signal to the predator that capturing the individual giving the alarm is more difficult than capturing its silent group members, as the caller is probably the most aware of the predator's location. In an aviary experiment using stuffed dummy Willow Tits Poecile montanus, we assessed whether an authentic alarm call given by Willow Tit affected Pygmy Owl Glaucidium passerinum prey preference. In the experiment, the Owls attacked only the ‘silent’ dummy individuals, suggesting that alarm calling could offer direct fitness benefits …
Environment-mediated morph-linked immune and life-history responses in the aposematic wood tiger moth
1. Warning signals are expected to evolve towards conspicuousness and monomorphism, and thereby hamper the evolution of multiple colour morphs. Here, we test fitness responses to different rearing densities to explain colour polymorphism in aposematic wood tiger moth (Parasemia plantaginis) males. 2. We used larval lines sired by white or yellow adult males selected for small or large melanization patterns of coloration. We reared these selected lines either solitarily (favourable conditions) or in aggregations (challenged conditions), and followed their performance to adult stage. We tested whether differences in larval density affected life-history traits, adult melanin expression, adult …
Electronic Supplementary Material from Ecological conditions alter cooperative behaviour and its costs in a chemically defended sawfly.
The evolution of cooperation and social behaviour is often studied in isolation from the ecology of organisms. Yet, the selective environment under which individuals evolve is much more complex in nature, consisting of ecological and abiotic interactions in addition to social ones. Here, we measured the life-history costs of cooperative chemical defence in a gregarious social herbivore, Diprion pini pine sawfly larvae, and how these costs vary under different ecological conditions. We ran a rearing experiment where we manipulated diet (resin content) and attack intensity by repeatedly harassing larvae to produce a chemical defence. We show that forcing individuals to allocate more to cooper…
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 a…
Changes in predator community structure shifts the efficacy of two warning signals in Arctiid moths
Summary 1. Polymorphism in warning coloration is puzzling because positive frequency-dependent selection by predators is expected to promote monomorphic warning signals in defended prey. 2. We studied predation on the warning-coloured wood tiger moth (Parasemia plantaginis )b y using artificial prey resembling white and yellow male colour morphs in five separate populations with different naturally occurring morph frequencies. 3. 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. 4. We found that yellow specimens were attacked less than white ones rega…
Data from: Ecological conditions alter cooperative behaviour and its costs in a chemically defended sawfly
The evolution of cooperation and social behaviour is often studied in isolation from the ecology of organisms. Yet, the selective environment under which individuals evolve is much more complex in nature, consisting of ecological and abiotic interactions in addition to social ones. Here we measured the life-history costs of cooperative chemical defence in a gregarious social herbivore, Diprion pini pine sawfly larvae, and how these costs vary under different ecological conditions. We ran a rearing experiment where we manipulated diet (resin content) and attack intensity by repeatedly harassing larvae to produce a chemical defence. We show that forcing individuals to allocate more to coopera…
Data from: Gray plumage color is more cryptic than brown in snowy landscapes in a resident color polymorphic bird
Camouflage may promote fitness of given phenotypes in different environments. The tawny owl (Strix aluco) is a colour polymorphic species with a grey and brown morph resident in the Western Palearctic. A strong selection pressure against the brown morph during snowy and cold winters has been documented earlier but the selection mechanisms remain unresolved. Here we hypothesise that selection favors the grey morph because it is better camouflaged against predators and mobbers in snowy conditions compared to the brown one. We conducted an online citizen science experiment where volunteers were asked to locate a grey or a brown tawny owl specimen from pictures taken in snowy and snowless lands…
Data from: Aposematism in the burying beetle? Dual function of anal fluid in parental care and chemical defense
Burying beetles (Nicrophorus vespilloides) bear distinctive and variable orange-black patterning on their elytra and produce an anal exudate from their abdomen when threatened. During breeding, the anal exudates contribute to the antimicrobial defense of the breeding resource. We investigated whether the anal exudates also provide a responsive chemical defense, which is advertised to potential avian predators by the beetle’s orange and black elytral markings. We found that that the orange-black elytral markings of the burying beetle are highly conspicuous for avian predators against range of backgrounds, by using computer simulations. Using bioassays with wood ants, we also showed that the …
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 25uC and 37uC 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 37uC increased bacterial…
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 o…