Predator-Induced Plasticity on Warning Signal and Larval Life-History Traits of the Aposematic Wood Tiger Moth, Arctia plantaginis

Correction Frontiers in Ecology and Evolution Volume 9 Article Number 737651 DOI 10.3389/fevo.2021.737651 Published JUL 29 2021Predator-induced plasticity in life-history and antipredator traits during the larval period has been extensively studied in organisms with complex life-histories. However, it is unclear whether different levels of predation could induce warning signals in aposematic organisms. Here, we investigated whether predator-simulated handling affects warning coloration and life-history traits in the aposematic wood tiger moth larva, Arctia plantaginis. As juveniles, a larger orange patch on an otherwise black body signifies a more efficient warning signal against predators but this comes at the costs of conspicuousness and thermoregulation. Given this, one would expect that an increase in predation risk would induce flexible expression of the orange patch. Prior research in this system points to plastic effects being important as a response to environmental changes for life history traits, but we had yet to assess whether this was the case for predation risk, a key driver of this species evolution. Using a full-sib rearing design, in which individuals were reared in the presence and absence of a non-lethal simulated bird attack, we evaluated flexible responses of warning signal size (number of orange segments), growth, molting events, and development time in wood tiger moths. All measured traits except development time showed a significant response to predation. Larvae from the predation treatment developed a more melanized warning signal (smaller orange patch), reached a smaller body size, and molted more often. Our results suggest plasticity is indeed important in aposematic organisms, but in this case may be complicated by the trade-off between costly pigmentation and other life-history traits.Peer reviewe

Safety in Numbers : How Color Morph Frequency Affects Predation Risk in an Aposematic Moth*

Polymorphic warning signals in aposematic systems are enigmatic because predator learning should favor the most common form, creating positive frequency-dependent survival. However, many populations exhibit variation in warning signals. There are various selective mechanisms that can counter positive frequency-dependent selection and lead to temporal or spatial warning signal diversification. Examining these mechanisms and their effects requires first confirming whether the most common morphs are favored at both local and regional scales. Empirical examples of this are uncommon and often include potentially confounding factors, such as a lack of knowledge of predator identity and behavior. We tested how bird behavior influences the survival of three coexisting morphs of the aposematic wood tiger moth Arctia plantaginis offered to a sympatric predator (great tit Parus major) at different frequencies. We found that although positive frequency-dependent selection is present, its strength is affected by predator characteristics and varying prey profitability. These results highlight the need to understand predator foraging in natural communities with variable prey defenses in order to better examine how behavioral interactions shape evolutionary outcomes.Peer reviewe

Geographic mosaic of selection by avian predators on hindwing warning colour in a polymorphic aposematic moth

Warning signals are predicted to develop signal monomorphism via positive frequency-dependent selection (+FDS) albeit many aposematic systems exhibit signal polymorphism. To understand this mismatch, we conducted a large-scale predation experiment in four countries, among which the frequencies of hindwing warning coloration of the aposematic moth,Arctia plantaginis,differ. Here we show that selection by avian predators on warning colour is predicted by local morph frequency and predator community composition. We found +FDS to be the strongest in monomorphic Scotland and lowest in polymorphic Finland, where the attack risk of moth morphs depended on the local avian community. +FDS was also found where the predator community was the least diverse (Georgia), whereas in the most diverse avian community (Estonia), hardly any models were attacked. Our results support the idea that spatial variation in predator communities alters the strength or direction of selection on warning signals, thus facilitating a geographic mosaic of selection.Peer reviewe

Adaptive Changes in Life History and Survival following a New Guppy Introduction

Numerous studies of wild populations have shown that phenotypic traits can change adaptively on short timescales, but very few studies have considered coincident changes in major fitness components. We here examine adaptive changes in life-history traits and survival rates for wild guppies introduced into new environments. Female life-history traits in the derived (Damier River) populations diverged from the ancestral (Yarra River) population, as a result of adaptation to predation regime (high vs. low) and other aspects of the local river. Moreover, some components of the derived Damier populations, particularly juveniles, now show higher survival in the Damier than do contemporary representatives from the ancestral Yarra population. These results suggest that adaptive change can improve survival rates after fewer than 10 years (fewer than 30 guppy generations) in a new environment

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 as a promising model to investigate multimodality in aposematic and sexual signaling. A. plantaginis is an aposematic diurnal moth which exhibits sexually dimorphic coloration as well as sex-limited polymorphism in part of its range. The anti-predator function of its coloration and, more recently, its chemical defenses (even when experimentally decoupled from the visual signals), has been well-demonstrated. Interestingly, recent studies have revealed differences between the two male morphs in mating success, suggesting a role of coloration in mate choice or attraction, and providing a possible explanation for its sexual dimorphism in coloration. Here, we: (1) review the lines of evidence showing the role of predation pressure and sexual selection in the evolution of multimodal aposematic signals in general, and in the wood tiger moth in particular; (2) establish gaps in current research linking sexual selection and predation as selective pressures on aposematic signals by reviewing a sample of the literature published in the last 30 years; (3) highlight the need of identifying suitable systems to address simultaneously the effect of natural and sexual selection on multimodal aposematic signals; and (4) propose directions for future research to test how aposematic signals can evolve under natural and sexual selection.Peer reviewe

Evolution of Male Coloration in The Wild: The Role of Sex Linkage and Selection

Male secondary sexual characters can be quite distinct, striking, and elaborate in nature. Despite many advances in the field of sexual selection, much remains to be known regarding why some organisms evolve these features more than others. Since Darwin published On the Origin of Species in 1859, many studies have measured the strength of natural selection in the wild showing that it is often strong and rapid (Both and Visser 2001; Pelletier et al. 2007; Kinnison et al. 2008; reviews: Hendry and Kinnison 1999; Reznick and Ghalambor 2001; Stockwell et al. 2003; Strauss et al. 2008; reviews: Endler 1986; Kingsolver et al. 2001; Hairston Jr. et al. 2005). Despite all these examples, a recent review has shown that very few of the traits measured in these studies involve secondary selected traits (Svensson and Gosden 2007). This is unfortunate because secondary selected traits often represent the most complex, elaborate traits in a variety of taxa including plants (eg. Geber, Dawson, and Delph 1998), insects (ex. Stubblefield and Seger 1994), fish (eg. Basolo and Trainor 2002), birds (eg. Hill and McGraw 2006), and reptiles (eg. Schulte-Hostedde and Schank 2009). Moreover, the evolution of one these particular traits in nature, male guppy coloration, represents one of our best examples of rapid evolution (Endler 1980). Adaptation requires both inheritance and selection, however most studies in rapid evolution either ignore heritability and concentrate on selective pressures or assume a particular mode of inheritance. Theoretical models have long established the importance of genetic architecture through sex linkage in sex-limited or sexually selected traits. However, empirical research in this topic is rare. In this thesis I present a comprehensive experimental study of how ecology and sex-linkage may interact to maintain the genetic variation and complex polymorphism in a sexually antagonistic, sex-limited trait in the wild. First I use a standard multivariate animal model to evaluate the heritability of two sub-traits of male coloration known to be linked to male fitness; orange and black body coloration. I also partition phenotypic variance of two introduced populations of guppies Poecilia reticulata) into its environmental and genetic components. The genetic components are then further partitioned into Y-linked versus non Y-linked variance to test the idea that sexually selected male traits are generally linked to the Y-chromosome where evolution is presumed to be faster as established by theory. I also studied genetic correlations among the two color patterns, and use all findings to predict the future trend of evolutionary change in this novel introduction. Using a quantitative genetics approach in this manner can help extract the genetic parameters affecting evolutionary change, and to my knowledge is the first study that separates Y-linked from non Y-linked quantitative genetic variance using a wild pedigree. Results show high proportion of Y-linked to non-Y linked genetic variance and that overall variation in Y-linkage accounts for most of the phenotypic variation in both introduction sites. Both sub-traits are also highly heritable and so combined with the abrupt change in selection pressure with the introduction I predict evolutionary change to be rapid in these populations. Second, following the results garnered in Chapter 1, here I track changes in adaptive divergence in both introduction sites bimonthly for one year post-introduction to see if our predictions were sound. My goal in this chapter was to investigate how variation in different selective pressures, such as predation and stream canopy cover, affect rates of divergence in a sexually selected polymorphic trait. Guppies were introduced from environments where they coexist with predators to two novel environments where there are no predators. In addition to the abrupt change in predation pressure, I also manipulated the canopy cover in one introduction site, hence doubling productivity in that environment. Results show rapid phenotypic and genotypic divergence in male coloration as expected, to date the fastest measure of change in wild guppies. Results also demonstrate that abrupt changes in habitat as well as predation-mediated mortality rates affect variation in rates of evolution of secondary sexual characters, an idea previously proposed but never formally tested. In the third Chapter I test the idea that microgeographic variation in sex-linkage occurs in multiple high- versus low-predation guppy populations, the first step needed to test theory regarding interactions between sex-linkage and selection. I examine a hypothesis that high-predation guppies have mainly Y-linkage of color patterns whereas low-predation guppies have color patterns linked to both the X- and Y-chromosome. In my thesis chapter I examine multiple high- and low-predation natural population using hormone assays in female guppies (which normally do not show coloration, and do not have a Y-chromosome) to test for differences in X-/autosomal linkage. I presume that changes in the amount of non-Y linked inheritance are combined with changes in Y-linkage. I also examine three introduction populations (from high- introduced into low predation sites) to see if these differences in linkage relationship respond rapidly to selection pressure. Results show that indeed low-predation guppies show a significantly higher amount of non-Y linked color patterns compared to high-predation guppies, and that this variation in linkage relationship can evolve in a matter of few guppy generations

Evolution of fitness in the wild

Environments are changing rapidly, which renders many local populations susceptible to extinction unless they can adapt to these changes. Studies of rapid adaptation commonly document the evolution of individual traits. Overall adaptation however, is a function of fitness itself, rather than the individual traits that contribute to fitness. Although numerous studies provide evidence for the evolution of specific traits on contemporary time scales, no published studies of wild animal populations have examined the evolution of a major fitness component following environmental change. My research demonstrates that an introduced population of guppies (Poecilia reticulata) has adapted to its new environment in less than ten years (13-26 generations). This adaptation consists of several phenotypic traits that have changed in the expected direction. Most critically, the introduced population now has higher survival than its ancestral source population when both are tested together in the introduction site. These results show that important components of fitness can evolve rapidly in populations, and that this evolution might influence the persistence of populations in the face of environmental change

Frequency-dependent flight activity in the colour polymorphic wood tiger moth

Predators efficiently learn to avoid one type of warning signal rather than several, making colour polymorphisms unexpected. Aposematic wood tiger moth males Parasemia plantaginis have either white or yellow hindwing coloration across Europe. Previous studies indicate that yellow males are better defended from predators, while white males have a positively frequency-dependent mating advantage. However, the potential frequency-dependent behavioural differences in flight between the morphs, as well as the role of male-male interactions in inducing flying activity, have not been previously considered. We ran an outdoor cage experiment where proportions of both male morphs were manipulated to test whether flying activity was frequencydependent and differed between morphs. The white morph was significantly more active than the yellow one across all treatments, and sustained activity for longer. Overall activity for both morphs was considerably lower in the yellow-biased environment, suggesting that higher proportions of yellow males in a population may lead to overall reduced flying activity. The activity of the yellow morph also followed a steeper, narrower curve than that of the white morph during peak female calling activity. We suggest that white males, with their presumably less costly defences, have more resources to invest in flight for predator escape and finding mates. Yellow males, which are better protected but less sexually selected, may instead compensate their lower flight activity by ‘flying smart’ during the peak female-calling periods. Thus, both morphs may be able to behaviourally balance the trade-off between warning signal selection and sexual selection. Our results emphasize the greater need to investigate animal behaviour and colour polymorphisms in natural or semi-natural environments [Current Zoology 61 (4): 765–772, 2015].peerReviewe