Resource specialization in a phytophagous insect: no evidence for genetically based performance trade‐offs across hosts in the field or laboratory

Abstract

We present a field test of the genetically based performance trade‐off hypothesis for resource specialization in a population of the moth Rothschildia lebeau whose larvae primarily feed on three host plant species. Pairwise correlations between growth vs. growth, survival vs. survival and growth vs. survival across the different hosts were calculated, using families (sibships) as the units of analysis. Of 15 pairwise correlations, 14 were positive, 5 significantly so and none were negative. The same pattern was found using complementary growth and survival data from the laboratory. Overall, we found no evidence of negative genetic correlations in cross‐host performance that would be indicative of performance trade‐offs in this population. Rather, variation among families in performance appears to reflect ‘general vigour’ whereby families that perform well on one host perform well across multiple hosts. We discuss the implications of positive genetic correlations in cross‐host performance in terms of the ecology and evolution of host range. We argue that this genetic architecture facilitates colonization of novel hosts and recolonization of historical hosts, therefore contributing to host shifts, host range expansions, biological invasions and introductions, and host ranges that are regionally broad but locally narrow.

Specialization and generalization in the diversification of phytophagous insects: tests of the musical chairs and oscillation hypotheses

“…The oscillation hypothesis also predicts that this trend towards specialization will drive speciation among generalist ancestral lineages. However, despite numerous attempts to measure fitness trade-offs among host-plant specialists and generalists, none has been identified; indeed, generalist species often have higher fitness than specialists across multiple hosts [41,42]. Contrary to expectations under the oscillation hypothesis, we recovered a strong negative relationship between hostplant breadth and diversification rate, both in a broad-scale analyses of Papilionoidea and a more narrowly focused analysis of Heliconiini, regardless of whether host breadth was treated as a binary or quantitative character.…”

Revisiting the evolution of ecological specialization, with emphasis on insect–plant interactions

“…Thus variation in performance among families suggests variation in general ''vigor'' but not host-specific trade-offs (Fry 1996). While these studies have most often used the least powerful designs (e.g., full-sib experiments; Camara 1997), the large number of times that investigators have tried and failed to find negative cross-host correlations in performance suggests that simple genetic trade-offs in performance are either rare or difficult to detect (Joshi and Thompson 1995, Whitlock 1996, Scriber 2005, Futuyma 2008, Agosta and Klemens 2009, Rasmann and Agrawal 2011. These conclusions are not without caveats that have been raised since Futuyma and Moreno (1988).…”

Scale insect host ranges are broader in the tropics

“…Many studies have looked for genetic trade-offs that would promote the evolution of host-plant specificity, and most have failed [2][3][4]25]. By contrast, the few studies that have tested ecological explanations for host-range variation have found strong support (e.g.…”

“…Adaptation to one host interferes with adaptations to another, and the jack of all trades is the master of none. However, there is little evidence that genetic trade-offs favour the evolution of host specialization: plant-feeding insect genotypes that do better on one host species also tend to do better on other host species [2][3][4], and comparative phylogenetic studies indicate that the cost of host-plant generalism may be much lower than expected [5]. Alternatively, host-range evolution may be primarily governed by ecological and population-genetic factors [6].…”