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. Here, we focused on the morph-linked reproductive costs of secretion of the abdominal fluid and quantified the proportion of phenotypic and genetic variation in it. We hypothesized that, if yellow males pay higher reproductive costs for their more effective aposematic display, the subsequent higher mating success of white males could offer one explanation for the maintenance of the polymorphism. We first found that the heritable variation in the quantity of abdominal secretion was very low (h2 = 0.006) and the quantity of defensive secretion was not dependent on the male morph. Second, deploying the abdominal defensive secretion decreased the reproductive output of both color morphs equally. This suggests that potential costs of pigment production and chemical defense against invertebrates are not linked in A. plantaginis. Furthermore, our results indicate that environmentally induced variation in chemical defense can alter an individual’s fitness significantly.

Evolutionary and ecological processes influencing chemical defense variation in an aposematic and mimeticHeliconiusbutterfly

“…Our broad-sense heritability estimate of biosynthesized cyanogenic toxicity (0.115 ± 0.086) is close to the average heritability value of physiological traits (0.12 ± 0.05), based on a meta-analysis of a wide range of traits and taxa (Hansen et al, 2011). This estimate differs markedly, though, from that obtained in a recent study on toxicity in warningly colored wood tiger moths (Arctia plantaginis), in which no evidence for a genetic component to variation in the secretion amounts of de novo synthesized chemical defenses could be detected (Burdfield-Steel et al, 2018;Lindstedt et al, 2020). A few other studies have estimated genetic components of insect chemical defense variation, with some detecting a genetic component (Eggenberger & Rowell-Rahier, 1992;Holloway et al, 1993;Yezerski et al, 2004) and others not (Müller et al, 2003).…”

“…The costs of producing and maintaining toxicity may also result in frequency-or density-dependent selection for resource optimization (Speed et al, 2012). Such costs could lead to energetic trade-offs (Bowers, 1992;Fordyce & Nice, 2008;Lindstedt et al, 2020) and automimicry (the occurrence of palatable "cheaters" in a chemically defended population; Brower et al, 1970;Speed et al, 2012). Evolutionary explanations for chemical defense variation are only plausible if such variation is genetically determined, and sufficient genetic variation is available for selection to act on.…”

Evolutionary and ecological processes influencing chemical defense variation in an aposematic and mimetic Heliconius butterfly

“…Our broad-sense heritability estimate of biosynthesized cyanogenic toxicity (0.115 ± 0.086) is close to the average heritability value of physiological traits (0.12 ±0.05), based on a meta-analysis of a wide range of traits and taxa (Hansen, Pélabon & Houle, 2011). This estimate differs markedly, though, from that obtained in a recent study on toxicity in warningly colored wood tiger moths (Arctia plantaginis), in which no evidence for a genetic component to variation in the secretion amounts of de novo synthesized chemical defenses could be detected (Burdfield-Steel et al, 2018;Lindstedt et al, 2020). A few other studies have estimated genetic components of insect chemical defense variation, with some detecting a genetic component (Eggenberger & Rowell-Rahier, 1992;Holloway, De Jong & Ottenheim, 1993;Yezerski, Gilmor & Stevens, 2004) and others not (Müller et al, 2003).…”

“…Variation in defenses can be maintained by frequency-dependent predator-mediated selection (Skelhorn & Rowe, 2005), or the costs of producing and maintaining toxicity resulting in frequency-or density-dependent selection in resource optimization and warning-signal honesty (Blount et al, 2009;Blount et al, 2012;Speed et al, 2012;Arenas, Walter & Stevens, 2015). Defense-related costs could lead to energetic trade-offs (Bowers, 1992;Fordyce & Nice, 2008;Lindstedt et al, 2020) and automimicry (the occurrence of palatable ''cheaters'' in a chemically defended population ;Brower, Pough & Meck, 1970;Speed et al, 2012). Evolutionary explanations for chemical defense variation are only plausible if such variation is genetically determined, and sufficient genetic variation is available for selection to act on.…”

Condition dependence in biosynthesized chemical defenses of an aposematic and mimetic Heliconius butterfly

“…Our result is contradictory with some studies on aposematic insects that find costs associated with chemical defenses. For instance, in the aposematic wood tiger moth Arctia plantaginis , the excretion of its defensive fluid (which contains also de novo synthesized compounds; Burdfield‐Steel et al, 2018 ) has negative consequences for reproductive output (Lindstedt et al, 2020 ). Handling/detoxifying of defensive compounds in its plant diet also comes at a cost to developmental traits and warning signal expression (Lindstedt et al, 2010 ; Reudler et al, 2015 ).…”