Alternative, intraspecific phenotypes offer an opportunity to identify the mechanistic basis of differences associated with distinctive life-history strategies. Wing dimorphic insects, in which both flight-capable and flight-incapable individuals occur in the same population, are particularly well-studied in terms of why and how the morphs trade-off flight for reproduction. Yet despite a wealth of studies examining the differences between female morphs, little is known about male differences, which could arise from different causes than those acting on females. Here we examined reproductive, gene expression, and biochemical differences between pea aphid (Acyrthosiphon pisum) winged and wingless males. We find that winged males are competitively superior in one-on-one mating circumstances, but wingless males reach reproductive maturity faster and have larger testes. We suggest that males tradeoff increased local matings with concurrent possible inbreeding for outbreeding and increased ability to find mates. At the mechanistic level, differential gene expression between the morphs revealed a possible role for activin and insulin signaling in morph differences; it also highlighted genes not previously identified as being functionally important in wing polymorphism, such as genes likely involved in sperm production. Further, we find that winged males have higher lipid levels, consistent with their use as flight fuel, but we find no consistent patterns of different levels of activity among five enzymes associated with lipid biosynthesis. Overall, our analyses provide evidence that winged versus wingless males exhibit differences at the reproductive, biochemical, and gene expression levels, expanding the field’s understanding of the functional aspects of morph differences.

There are three sections of these data relating to each figure of the manuscript. The first section (figure 1) includes developmental timing, testes area, and mating success data. The second section (figure 2) comes from a 2014 RNAseq experiment and all the sequence data is on NCBI (list of SRA accessions included here), and the pipeline and DEseq data are present. Lastly, the final section (figure 3) includes lipid and enzyme assays.