Abstract
The whitefly Bemisia tabaci is a closely related group of >35 cryptic species that feed on the phloem sap of a broad range of host plants. Species in the complex differ in their host‐range breadth, but the mechanisms involved remain poorly understood. We investigated, therefore, how six different B. tabaci species cope with the environmental unpredictability presented by a set of four common and novel host plants. Behavioral studies indicated large differences in performances on the four hosts and putative specialization of one of the species to cassava plants. Transcriptomic analyses revealed two main insights. First, a large set of genes involved in metabolism (>85%) showed differences in expression between the six species, and each species could be characterized by its own unique expression pattern of metabolic genes. However, within species, these genes were constitutively expressed, with a low level of environmental responsiveness (i.e., to host change). Second, within each species, sets of genes mainly associated with the super‐pathways “environmental information processing” and “organismal systems” responded to the host switching events. These included genes encoding for proteins involved in sugar homeostasis, signal transduction, membrane transport, and immune, endocrine, sensory and digestive responses. Our findings suggested that the six B. tabaci species can be divided into four performance/transcriptomic “Types” and that polyphagy can be achieved in multiple ways. However, polyphagy level is determined by the specific identity of the metabolic genes/pathways that are enriched and overexpressed in each species (the species' individual metabolic “tool kit”).
Highlights
Herbivorous insects exhibit a wide range of feeding-strategy interactions with their plant hosts, with the classic main division distinguishing between generalist and specialist habits
We extended our analyses to the full transcriptomes of the same six B. tabaci species, in order to understand the highlevel functional differences between the selected species and to identify the molecular mechanisms that might explain the huge variability in host adaptation among the species in the complex
Within the 85% constitutively expressed genes, each species displayed its own unique expression pattern of metabolic genes. These findings suggest that polyphagy can be achieved in multiple ways in B. tabaci, but its level is determined by the specific identity of the metabolic genes/pathways that are enriched and overexpressed in each species, together with the expression levels of non-metabolic genes in response to novel host plants
Summary
Herbivorous insects exhibit a wide range of feeding-strategy interactions with their plant hosts, with the classic main division distinguishing between generalist and specialist habits. As it is agreed that generalism is quite rare (Jaenike, 1990), its presence within certain lineages can be hypothesized to associate with a unique set of largely unknown and restricted biological attributes (mechanisms) that promote the evolution of generalist lineages (Clarke, 2017) It is widely believed, for example, that generalists and specialists insect herbivores differ in the strategies they use to cope with plants' secondary defense compounds (Ali & Agrawal, 2012; HeidelFischer & Vogel, 2015; Vogel et al, 2014b). The nutrient intake space of both generalist and specialist phloem-feeding insects is very different from that described above, as these species need to cope with a poor diet that contains high levels of sugar with low levels of essential components such as amino acids (Douglas, 2006). These findings suggest that polyphagy can be achieved in multiple ways in B. tabaci, but its level is determined by the specific identity of the metabolic genes/pathways that are enriched and overexpressed in each species (the species' individual metabolic “tool kit”), together with the expression levels of non-metabolic genes in response to novel host plants
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