Positive Frequency-Dependent Selection on Warning Color in Alpine Leaf Beetles

Borer, Matthias; Noort, Tom van; Rahier, Martine; Naisbit, Russell E.

doi:10.1111/j.1558-5646.2010.01137.x

Cited by 59 publications

(77 citation statements)

References 24 publications

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“…Experiments in the laboratory (13,14) and in natural contexts (15)(16)(17)(18) have demonstrated that naive predators have the cognitive capabilities to associate conspicuous signals with toxicity, and to avoid them later. Transplant experiments with live prey or artificial prey models performed in the field have shown increased survival for prey matching the locally abundant warning signal and lower fitness for prey with exotic or novel signals, explaining the stable geographic mosaic of locally uniform warning signals observed (16,17,(19)(20)(21).However, selection favoring mimicry in those studies takes on the pattern of purifying selection for local signals (15,17,20), so the role of positive FDS in the evolution of mimicry is unclear. Indeed, distinguishing the effect of positive FDS from local purifying selection is particularly challenging because the polymorphism necessary to distinguish between them is intrinsically unstable when the most common forms are favored (15-17, 20, 22).…”

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“…However, selection favoring mimicry in those studies takes on the pattern of purifying selection for local signals (15,17,20), so the role of positive FDS in the evolution of mimicry is unclear. Indeed, distinguishing the effect of positive FDS from local purifying selection is particularly challenging because the polymorphism necessary to distinguish between them is intrinsically unstable when the most common forms are favored (15-17, 20, 22).…”

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Warning signals are under positive frequency-dependent selection in nature

Chouteau

Arias

Joron

2016

Proc. Natl. Acad. Sci. U.S.A.

147

168

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Positive frequency-dependent selection (FDS) is a selection regime where the fitness of a phenotype increases with its frequency, and it is thought to underlie important adaptive strategies resting on signaling and communication. However, whether and how positive FDS truly operates in nature remains unknown, which hampers our understanding of signal diversity. Here, we test for positive FDS operating on the warning color patterns of chemically defended butterflies forming multiple coexisting mimicry assemblages in the Amazon. Using malleable prey models placed in localities showing differences in the relative frequencies of warningly colored prey, we demonstrate that the efficiency of a warning signal increases steadily with its local frequency in the natural community, up to a threshold where protection stabilizes. The shape of this relationship is consistent with the direct effect of the local abundance of each warning signal on the corresponding avoidance knowledge of the local predator community. This relationship, which differs from purifying selection acting on each mimetic pattern, indicates that predator knowledge, integrated over the entire community, is saturated only for the most common warning signals. In contrast, among the well-established warning signals present in local prey assemblages, most are incompletely known to local predators and enjoy incomplete protection. This incomplete predator knowledge should generate strong benefits to life history traits that enhance warning efficiency by increasing the effective frequency of prey visible to predators. Strategies such as gregariousness or niche convergence between comimics may therefore readily evolve through their effects on predator knowledge and warning efficiency.Müllerian mimicry | aposematism | warning signal | predation | butterflies F requency-dependent selection (FDS) occurs when the fitness of a phenotype depends on its frequency in the population (1). Under negative FDS, the fitness of a phenotype will decrease as its frequency increases. This supposedly common mechanism (2) maintains adaptive polymorphism and has been documented in a variety of natural systems, ranging from foraging behavior (2, 3) and pollination syndromes (4) to predator-prey (5-7) and parasite-host coevolution (8). On the other hand, positive FDS is a selection regime where the fitness of a phenotype increases with its frequency and does not readily maintain polymorphism. However, positive FDS is thought to be a mechanism central to the evolution of a large diversity of adaptive strategies. Notably, traits used in signaling and communication, where efficiency depends on local frequency, such as languages and social signals (9), flower coloration for pollinator attraction (10), and warning signals of prey unpalatability (11), should be subjected to positive FDS. However, although the principles of positive FDS may be well understood from a theoretical point of view, the extent to which it is operating in nature remains largely unknown.Warning coloration advertising ...

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Warning signals are under positive frequency-dependent selection in nature

Chouteau

Arias

Joron

2016

Proc. Natl. Acad. Sci. U.S.A.

147

168

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“…The potential that the many migratory species of birds that visit northerly areas widely generalize their avoidance of aposematic taxa by general cues also exists (i.e., avoiding anything with bright conspicuous colors or patterns). Some work on alpine borer beetles in Europe has shown evidence of positive FDS (Borer et al 2010), but work on the wood tiger moth has not (Nokelainen 2013, Hegna et al 2013a). …”

Section: Frequency-dependent Selectionmentioning

confidence: 99%

“…Some of the species found to have geographically varying warning signals include Neotropical Heliconius butterflies (Brown & Benson 1974, Brower 1996, Mallet 2010, ladybird beetles (Creed 1966, Brakefield 1985, Dolenská et al 2009, Blount et al 2012, monarch butterflies (Brower 1958, Davis et al 2005, Davis et al 2012, newts (Mochida 2009, Mochida 2011, poison frogs (Daly & Myers 1967, Savage 1968, Summers et al 2003, Wang & Summers 2010, Wang 2011, Rudh et al 2011, Maan & Cummings 2012, Willink et al 2013, RichardsZawacki et al 2013, Hegna et al 2013b), velvet ants (Wilson et al 2012), alpine leaf beetles (Borer et al 2010), and bumble bees (Plowright & Owen 1980). Interestingly, some aposematic species appear to switch between aposematic and cryptic strategies across their distributions.…”

Section: Geographic Variation For Different Preymentioning

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Influences of geographic differentiation in the forewing warning signal of the wood tiger moth in Alaska

Hegna

Mappes

2014

Evol Ecol

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Geographic Variation in the WarningSignals of the Wood Tiger Moth (Parasemia plantaginis; Arctiidae)Esitetään Jyväskylän yliopiston matemaattis-luonnontieteellisen tiedekunnan suostumuksella julkisesti tarkastettavaksi yliopiston Ylistönrinteellä, salissa YAA303 marraskuun 8. päivänä 2013 kello 12.Academic dissertation to be publicly discussed, Warning signals are not expected to be diverse because they are under stabilizing selection. This dissertation aims to study historic and contemporary selection mechanisms underlying the geographic warning signal diversity in the wood tiger moth (Parasemia plantaginis). In the first study, I explored the variation in hindwing warning color frequencies across the distribution of P. plantaginis and the phylogeography of the species. Males have polymorphic hindwing color (yellow or white) across much of their distribution but turn reddish in the Caucasus and mostly white in Japan, which coincide with mitogenetic divergence. Females vary continuously in hindwing warning color between yellow and red, becoming yellow east of the Ural mountain range, but does not correspond to mitogenetic divergence. Post-glacial isolation may be one contributing factor to the genetic divergence and the hindwing warning signal differences in the Caucasus region. In the second study, I found that thermoregulation benefits of melanin can trade-off with a larger more effective warning signal, which contributes to variation in melanization within Europe. In the third study, I found that forewing patterns function as warning signals and that generalization by predators might play an important role in warning signal diversity along with frequency dependent selection. In the fourth chapter, I found three populations in Japan differing in warning signal traits with some gene flow suggesting both selection and isolation may be underlying causes. Overall, my results suggest that historical and abiotic factors contribute to the observed warning signal diversity in P. plantaginis, rather than predation alone. This adds to our understanding of how historical factors along with environmental heterogeneity in biotic and abiotic factors can promote warning signal diversity. My results highlight the need to take an integrated approach to studying geographic diversity in warning signals.

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Using Delaunay triangulation to sample whole‐specimen color from digital images

Valvo

Aponte

Daniel

et al. 2021

Ecology and Evolution

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Color variation is one of the most obvious examples of variation in nature, but biologically meaningful quantification and interpretation of variation in color and complex patterns are challenging. Many current methods for assessing variation in color patterns classify color patterns using categorical measures and provide aggregate measures that ignore spatial pattern, or both, losing potentially important aspects of color pattern. Here, we present Colormesh, a novel method for analyzing complex color patterns that offers unique capabilities. Our approach is based on unsupervised color quantification combined with geometric morphometrics to identify regions of putative spatial homology across samples, from histology sections to whole organisms. Colormesh quantifies color at individual sampling points across the whole sample. We demonstrate the utility of Colormesh using digital images of Trinidadian guppies (Poecilia reticulata), for which the evolution of color has been frequently studied. Guppies have repeatedly evolved in response to ecological differences between up‐ and downstream locations in Trinidadian rivers, resulting in extensive parallel evolution of many phenotypes. Previous studies have, for example, compared the area and quantity of discrete color (e.g., area of orange, number of black spots) between these up‐ and downstream locations neglecting spatial placement of these areas. Using the Colormesh pipeline, we show that patterns of whole‐animal color variation do not match expectations suggested by previous work. Colormesh can be deployed to address a much wider range of questions about color pattern variation than previous approaches. Colormesh is thus especially suited for analyses that seek to identify the biologically important aspects of color pattern when there are multiple competing hypotheses or even no a priori hypotheses at all.

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Positive Frequency-Dependent Selection on Warning Color in Alpine Leaf Beetles

Cited by 59 publications

References 24 publications

Warning signals are under positive frequency-dependent selection in nature

Warning signals are under positive frequency-dependent selection in nature

Influences of geographic differentiation in the forewing warning signal of the wood tiger moth in Alaska

Using Delaunay triangulation to sample whole‐specimen color from digital images

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