Phylogenetic relatedness and host plant growth form influence gene expression of the polyphagous comma butterfly (Polygonia c-album)

Abstract

Background: The mechanisms that shape the host plant range of herbivorous insect are to date not well understood but knowledge of these mechanisms and the selective forces that influence them can expand our understanding of the larger ecological interaction. Nevertheless, it is well established that chemical defenses of plants influence the host range of herbivorous insects. While host plant chemistry is influenced by phylogeny, also the growth forms of plants appear to influence the plant defense strategies as first postulated by Feeny (the "plant apparency" hypothesis). In the present study we aim to investigate the molecular basis of the diverse host plant range of the comma butterfly (Polygonia c-album) by testing differential gene expression in the caterpillars on three host plants that are either closely related or share the same growth form.

Results: In total 120 genes were identified to be differentially expressed in P. c-album after feeding on different host plants, 55 of them in the midgut and 65 in the restbody of the caterpillars. Expression patterns could be confirmed with an independent method for 14 of 27 tested genes. Pairwise similarities in upregulation in the midgut of the caterpillars were higher between plants that shared either growth form or were phylogenetically related. No known detoxifying enzymes were found to be differently regulated in the midgut after feeding on different host plants.

Conclusion: Our data suggest a complex picture of gene expression in response to host plant feeding. While each plant requires a unique gene regulation in the caterpillar, both phylogenetic relatedness and host plant growth form appear to influence the expression profile of the polyphagous comma butterfly, in agreement with phylogenetic studies of host plant utilization in butterflies.

Figure 1

General patterns of gene expression in the larval midgut of Polygonia c-album. Dark grey represent qualitative differences or similarities (present/absent), light grey represent quantitative differences or similarities (more/less). (a) The number of uniquely upregulated genes on the three host plants used in the study, showing that significantly fewer genes were uniquely upregulated on Ulmus. (b) Pairwise similarities in upregulation between two of the three host plants. "Urticalean rosids" = Urtica dioica + Ulmus glabra; "Trees" = Ulmus glabra + Salix caprea; "No connection" = Urtica dioica + Salix caprea. Following predictions, more genes were concurrently upregulated on plants that shared either ancestry or growth form.

Figure 2

General patterns of gene expression in the larval restbody of Polygonia c-album. Dark grey represent qualitative differences or similarities (present/absent), light grey represent quantitative differences or similarities (more/less). The pattern seen in the restbody is distinctly different from the midgut. (a) The number of uniquely upregulated genes on the three host plants used in the study. (b) Pairwise similarities in upregulation between two of the three host plants. "Urticalean rosids" = Urtica dioica + Ulmus glabra; "Trees" = Ulmus glabra + Salix caprea; "No connection" = Urtica dioica + Salix caprea. Again, the pattern is different from the midgut; there are no effects of shared ancestry or growth form.

Figure 3

Correlation between preference and performance in Polygonia c-album. Correlation between relative oviposition preference (degree of preference in simultaneous choice trials) and larval performance (mean growth rate) for the plants used in the present study (means ± SE). Data from [34].