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

Abstract

Our understanding of how novel warning color traits evolve in natural populations is largely based on studies of reproductive stages and organisms with endogenously produced pigmentation. In these systems, genetic drift is often required for novel alleles to overcome strong purifying selection stemming from frequency-dependent predation and positive assortative mating. Here, we integrate data from field surveys, predation experiments, population genomics, and phenotypic correlations to explain the origin and maintenance of geographic variation in a diet-based larval pigmentation trait in the redheaded pine sawfly (Neodiprion lecontei), a pine-feeding hymenopteran. Although our experiments confirm that N. lecontei larvae are indeed aposematic-and therefore likely to experience frequency-dependent predation-our genomic data do not support a historical demographic scenario that would have facilitated the spread of an initially deleterious allele via drift. Additionally, significantly elevated differentiation at a known color locus suggests that geographic variation in larval color is currently maintained by selection. Together, these data suggest that the novel white morph likely spread via selection. However, white body color does not enhance aposematic displays, nor is it correlated with enhanced chemical defense or immune function. Instead, the derived white-bodied morph is disproportionately abundant on a pine species with a reduced carotenoid content relative to other pine hosts, suggesting that bottom-up selection via host plants may have driven divergence among populations. Overall, our results suggest that life stage and pigment source can have a substantial impact on the evolution of novel warning signals, highlighting the need to investigate diverse aposematic taxa to develop a comprehensive understanding of color variation in nature.

Multiple mechanisms contribute to isolation-by-environment in the redheaded pine sawfly, Neodiprion lecontei

“…A large dataset of SNP markers was prepared using the same extraction and doubledigest RAD (ddRAD) sequencing approaches described in Lindstedt et al (2022) and Bendall et al (2022). Briefly, 58 Arboretum individuals prepared following a modified version of the original ddRAD protocol (B. K. Peterson et al, 2012), and labeled with one of 48 unique, variable-length (Burford Reiskind et al, 2016) in-line barcodes during adapter ligation (Supplemental Tables S3, S4).…”

Body size as a magic trait in two plant-feeding insect species

“…Similarly, cryptic Cephalelus uncinatus leafhoppers avoid avian predation by resting on host plants with stems that match their body size: larger individuals are always found on plants with thicker stems, while smaller individuals are found on plants with thinner stems (Augustyn et al 2017). By contrast, in aposematic species such as N. lecontei and N. pinetum (Lindstedt et al 2022), having a larger visual signal (either via larger bodies or larger groups) may enhance predator avoidance learning (Mappes and Alatalo 1997;Gamberale and Tullberg 1998;Forsman and Merilaita 1999;Riipi et al 2001). However, group or individual size may be limited by physical properties of the host.…”

Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: Simulations and empirical data from pine‐feeding hymenopterans

“…While N. pinetum and N. lecontei share many similarities, N. pinetum feeds exclusively on white pine (Pinus strobus) and N. lecontei tends to avoid this host. Differences between their hosts probably generate divergent selection on many different larval and adult traits (Bendall et al, 2017;Codella & Raffa, 2002;Coppel & Benjamin, 1965;Lindstedt et al, 2022). For example, differences in needle chemistry and thickness between the preferred hosts of N. lecontei and N. pinetum are associated with differences in egg size, female ovipositor morphology and female egg-laying behaviours.…”

“…lecontei tends to avoid this host. Differences between their hosts probably generate divergent selection on many different larval and adult traits (Bendall et al, 2017; Codella & Raffa, 2002; Coppel & Benjamin, 1965; Lindstedt et al, 2022). For example, differences in needle chemistry and thickness between the preferred hosts of N .…”