Appearance before performance? Nutritional constraints on life‐history traits, but not warning signal expression in aposematic moths

Abstract

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 coloration. We studied this with an aposematic herbivore Arctia plantaginis (Arctiidae), whose larvae and adults show extensive variation in aposematic coloration. In larvae, less melanic coloration (i.e. larger orange patterns) produces a more efficient warning signal against predators, whereas high amounts of melanism (smaller orange pattern) enhance thermoregulation, correlate with better immunity and make individuals harder to detect for naïve predators. We conducted a factorial rearing experiment with larvae originating from lines selected for either small or large orange signal size, which were reared on an artificial diet that had either low or high protein content. Protein content of the diet is critical for melanin production. We measured the effects of diet on individual coloration, life‐history traits, immune defence and reproductive output. We also compared the responses to dietary conditions between the small and large larval signal genotypes. Protein content of the diet did not affect warning coloration in the larval stage, but larval signal sizes differed significantly among selection lines, confirming that its variation is mainly genetically determined. In adults, signal line or diet did not affect coloration in hindwings, but males' forewings had more melanin on the high than on low protein diet. Contrary to coloration, diet quality had a stronger impact on life‐history traits: individuals developed for longer had smaller hindwing sizes in females and lower immune defence on the low protein content diet compared with the high. These costs were higher for more melanic larval signal genotypes in terms of development time and female hindwing size. We conclude that low plasticity in warning signal characteristics makes signal expression robust under varying dietary conditions. Therefore, variation in diet quality is not likely to constrain signal expression, but can have a bigger impact on performance.

The impact of life stage and pigment source on the evolution of novel warning signal traits

“…Nevertheless, larvae are conspicuous on all three hosts and in the absence as immune defense (36,(47)(48)(49)(50), trade-offs between warning signaling and these other functions could result in divergent selection on pigmentation on different host plants. These trade-offs and constraints should be most evident when the availability of pigments or their precursors are limited in the diet (19). However, such trade-offs should also generate genetic correlations between levels of carotenoid-based pigmentation and other fitness traits (especially immune or antioxidant function), which we did not find in this study (Table 3, see also (88) (27,35,46,89).…”

“…Less efficient warning signal forms can also be favored under certain dietary conditions (18)(19)(20) or maintained via genetic correlations with other traits through physical linkage or pleiotropy (21). Importantly, these three scenarios (neutrality, purifying selection, and positive selection) are not mutually exclusive and the origin and spread of novel color alleles could be facilitated by a combination of genetic drift under relaxed selection, followed by positive selection (12)(13)(14).…”

“…Bottom-up selection may have an especially strong impact in herbivorous species, for which variation in host-plant use across space can lead to differences in access to defensive compounds acquired from the host (39), the visual background against which coloration is displayed (40), and access to diet-derived pigments (41). While host shifts may also impact the availability of nutrients needed to produce pigments endogenously, warning signals based on endogenous pigments seem to be more robust and less variable under nutritional stress (19). As a consequence, spatial variation in diet quality and nutrient availability is hypothesized to have a much stronger impact on diet-derived warning signal pigmentation than on endogenously produced pigments (36).…”

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

“…and kept under greenhouse temperatures that followed the outdoor temperature, between 20 and 30 • C during the day (∼20 h) and 15-20 • C during the night (∼4 h). In Finland, this species usually has one generation per year and A. plantaginis typically overwinter as a 3rd or 4th instar larva (Lindstedt et al, 2019).…”

Batesian mimicry has evolved with deleterious effects of the pleiotropic gene doublesex

“…Although the evolution of Batesian mimicry has endowed the selective advantage of reduced predation, it may also be associated with physiological trade-offs, which may affect the establishment and maintenance of female-limited polymorphism 9,10 . The evolution and maintenance of colour polymorphism to avoid predation have been studied in diverse contexts, such as natural selection, sexual selection, and life-history trade-offs [11][12][13][14] . In female-limited polymorphic mimicry, negative frequency-dependent selection (NFDS), through which the advantage of mimetic forms decreases as their frequency increases, is indispensable to maintain polymorphism 10 .…”