Genetic Basis of Body Color and Spotting Pattern in Redheaded Pine Sawfly Larvae (Neodiprion lecontei)

Abstract

Pigmentation has emerged as a premier model for understanding the genetic basis of phenotypic evolution, and a growing catalog of color loci is starting to reveal biases in the mutations, genes, and genetic architectures underlying color variation in the wild. However, existing studies have sampled a limited subset of taxa, color traits, and developmental stages. To expand the existing sample of color loci, we performed QTL mapping analyses on two types of larval pigmentation traits that vary among populations of the redheaded pine sawfly (Neodiprion lecontei): carotenoid-based yellow body color and melanin-based spotting pattern. For both traits, our QTL models explained a substantial proportion of phenotypic variation and suggested a genetic architecture that is neither monogenic nor highly polygenic. Additionally, we used our linkage map to anchor the current N. lecontei genome assembly. With these data, we identified promising candidate genes underlying (1) a loss of yellow pigmentation in populations in the mid-Atlantic/northeastern United States [C locus-associated membrane protein homologous to a mammalian HDL receptor-2 gene (Cameo2) and lipid transfer particle apolipoproteins II and I gene (apoLTP-II/I)], and (2) a pronounced reduction in black spotting in Great Lakes populations [members of the yellow gene family, tyrosine hydroxylase gene (pale), and dopamine N-acetyltransferase gene (Dat)]. Several of these genes also contribute to color variation in other wild and domesticated taxa. Overall, our findings are consistent with the hypothesis that predictable genes of large effect contribute to color evolution in nature.

Keywords: carotenoids; convergent evolution; evolutionary genetics; genetic architecture; melanin; pigmentation.

Figure 1

Interspecific variation in Neodiprion larval color. Top row (left to right): Neodiprion nigroscutum, N. rugifrons, N. virginianus. Middle row (left to right): N. pinetum, N. lecontei, N. merkeli. Bottom row (left to right): N. pratti, N. compar, N. swainei. Larvae in the first and last columns are exhibiting a defensive U-bend posture (a resinous regurgitant is visible in N. virginianus, top right). N. pratti photo is by K. Vertacnik, all others are by R. Bagley.

Figure 2

Intraspecific variation in Neodiprion lecontei larval color and cross design. We crossed yellow, light-spotted haploid males from MI to white, dark-spotted diploid females from VA. This produced haploid males with the VA genotype and phenotype (data not shown) and diploid females (F₁) with intermediate spotting and color. Virgin F₁ females produced recombinant haploid males (F₂) with a wide range of body color and spotting pattern (a representative sample is shown).

Figure 3

Larval color variation among N. lecontei populations and across generations. For larval body color (A–C), higher scores for yellow (A) and lower scores for PC1 (B) and PC2 (C) indicate higher levels of yellow pigment. For larval spotting pattern (D–E), higher spot numbers (D) and spot area scores (E) indicate more melanic spotting. For all traits, boxes represent interquartile ranges (median ± 2 SD), with outliers indicated as points. For each trait (A–E), lowercase letters indicate which comparisons differ significantly after correction for multiple comparisons (see Table S3 in File S1 for full statistical results).

Figure 4

N. lecontei linkage map with larval color QTL and 1.5 LOD support intervals.

Figure 5

LOD profiles and interaction plots for larval color traits. Interval mapping analyses recovered QTL for larval body color (Yellow, PC1, PC2) on linkage groups 1, 2, 3, and 5 (A) and a single QTL × QTL interaction (B). QTL for larval spotting pattern (spot area and spot number) were on linkage groups 2 and 6 (C), with three QTL × QTL interactions (D). QTL names are as in Table 1.