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

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 the evolution of novel
warning signals, highlighting the need to investigate diverse aposematic
taxa to develop a comprehensive understanding of color variation in
nature.