The project focuses on elucidating the development of the weevil head capsule, in particular the elongate snout, a structure that is implicated in their considerable evolutionary success. Key weevil species critical in agriculture, forestry, and/or horticulture will be investigated for the formation of the snout, used in producing holes for feeding or egg deposition in plant tissues. This project will resolve those genetic elements responsible for snout formation and alterations in its overall structure, as well as the timing of episodes of diversification. It will also provide the first comprehensive consideration of weevil evolution and those factors driving their success.

Weevils rank among the most diverse of all organisms, with around 60,000 species. They are of extreme economic importance owing to their impact on natural and agricultural ecosystems, damaging all major groups of plants and representing one of the most serious lineages of arthropod pests. Resolution of those factors that have led to the remarkable diversity of weevils will permit a refined understanding of their specialization on different plant families and tissues. Insight into those genetic factors which have fueled their diversification and evolutionary success will develop new avenues for research in biological control as well as fundamentals of weevil biology.

Project Report

The project spanned multidisciplinary avenues of research to resolve long-standing issues regarding the evolution of weevils (Fig. 1), one of the most ecologically unbiquitous of plant-feeding beetles and with a modern diversity of about 50,000 species. We united data from paleontology, comparative morphology, developmental biology, histology, and genomics to arrive at a comprehensive perspective on the diversification of weevils through time, as well as develop an understanding of the origin, mechanism of formation, genetic architecture, and diversity of the characteristic weevil rostrum, an evolutionary novelty widely supported as a key innovation in the success of these beetles. The rostrum, an elongation of head head capsule beyond the compound eyes, is used to access a variety of plant tissues and to uniquely create cavities in which to lay and conceal their eggs. Today weevils are one of the most injuious of beetle groups in agricultural ecosystems worldwide. Any understanding of the factors that have led to their tremendous success provides us with a more holistic perspective on their evolution and potential control. Our results, stemming from paleontology, comparative morphology, histology, and developmental biology, demonstrate a Jurassic origin for weevils, with multiple waves of diversification throughout the last 200 million years. The earliest weevils, whose modern-day relatives in the relic family Nemonychidae, dominated the fauna until the Early Cretaceous at which time additional families among the weevils begin to appear (such as the family Caridae and primitive members of other lineages including the hyperdiverse Curculionidae). The Curculionidae itself appears to have had its greatest diversification around the time of the radiation of flowering plants in the middle Cretaceous. Histological examination of the developing and adult rostrum (Figs. 5, 6) revealed a wide variety of important character data for understanding not only its formation but resolution of controversial relationships among weevils, particularly in relation to the bark and ambrosia beetles. Genomic work on the formation of the weevil rostrum reveal a set of genes involved in the formation and modification of this structure. Whole genomic data was used to localize a suite of genes which played a role in rostrum development. From this subst of genes, knock-out experiments (RNAi) were undertaken to elucidate the individual functions of each gene or gene set. For example, the gene set known as 'Broad Complex' appears to mostly eliminate rostrum formation altogether (Fig. 4, normal rostrum depicted in figure 1), while others modify the overall form in sundry manners (Figs. 2, 3). Indeed, by manipulating the expression of particular genes, it was possible to remove many of the evolutionarily derived features in a higher weevil and alternatively express the ancestral state that exists either in the most primitive of weevils today or would have been found in a proto-weevil ancestor. This has permitted us to identify the genetic architecture associated with the formation of this evolutionary novelty, one that appeared around 200 million years ago. By identifying the time in which this novelty first appeared we have been able to accurately place for the first time this genetic alteration into the paleoecological and paleoclimatology context in which it first developed.

National Science Foundation (NSF)
Division of Environmental Biology (DEB)
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David Mindell
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University of Kansas
United States
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