Evaluating responses to temperature during pre-metamorphosis and carry-over effects at post-metamorphosis in the wood tiger moth (Arctia plantaginis)

Abstract

Insect metamorphosis is one of the most recognized processes delimiting transitions between phenotypes. It has been traditionally postulated as an adaptive process decoupling traits between life stages, allowing evolutionary independence of pre- and post-metamorphic phenotypes. However, the degree of autonomy between these life stages varies depending on the species and has not been studied in detail over multiple traits simultaneously. Here, we reared full-sib larvae of the warningly coloured wood tiger moth ( Arctia plantaginis ) in different temperatures and examined their responses for phenotypic (melanization change, number of moults), gene expression (RNA-seq and qPCR of candidate genes for melanization and flight performance) and life-histories traits (pupal weight, and larval and pupal ages). In the emerging adults, we examined their phenotypes (melanization and size) and compared them at three condition proxies: heat absorption (ability to engage flight), flight metabolism (ability to sustain flight) and overall flight performance. We found that some larval responses, as evidenced by gene expression and change in melanization, did not have an effect on the adult (i.e. size and wing melanization), whereas other adult traits such as heat absorption, body melanization and flight performance were found to be impacted by rearing temperature. Adults reared at high temperature showed higher resting metabolic rate, lower body melanization, faster heating rate, lower body temperature at take-off and inferior flight performance than cold-reared adults. Thus, our results did not unambiguously support the environment-matching hypothesis. Our results illustrate the importance of assessing multiple traits across life stages as these may only be partly decoupled by metamorphosis. This article is part of the theme issue ‘The evolution of complete metamorphosis'.

Complete metamorphosis of insects

“…Decoupling can also be tested at the level of the phenotype. Using the wood tiger moth, Galarza et al [68] investigated the decoupling of a suite of traits including life-history traits, morphological traits and in gene expression between larva and adults. Depending on the traits, they found decoupling but also carry-over effects from the larval to the adult phenotype driven by the experimentally changed royalsocietypublishing.org/journal/rstb Phil.…”

Comparative transcriptome analysis of the rice leaf folder (Cnaphalocrocis medinalis) to heat acclimation

“…Temperature also affects insect behaviours, such as feeding [3], flight and walking [10], host choice, settling and folding leaf behaviours [11]. Changes in temperature also result in deficiency or abnormality of insects in respiration, nervous, metabolism, and endocrine systems [12][13][14]. The ventilatory rhythm frequency of the locust Locusta migratoria increases with the increase of temperature [12].…”

“…The ventilatory rhythm frequency of the locust Locusta migratoria increases with the increase of temperature [12]. The resting metabolic rates of the wood tiger moths Arctia plantaginis are significantly higher when larvae reared at 25°C than that at 16°C [13]. Temperature affects invertebrate hormone system, and the increased temperature induces expression of endocrine signaling genes of chironomids Chironomus riparius [14].…”

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

“…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).…”

“…As a result, this can further strengthen selection against novel warning signal forms (30,32). By contrast, because coloration tends to be decoupled across ontogeny (28,34,35) but see (21), aposematic larvae are not usually subject to direct sexual selection. Thus, all else equal, we hypothesize that the cost of being a rare aposematic color allele may be lessened in the larval stage, making the evolutionary shift to a novel color morph comparatively easier for larvae.…”