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

Subject Areas: evolution 2 Authors for correspondence: Nate B. Hardy e-mail: Sarah P. Otto e-mail: 2 Nate B. Hardy 1 2 Sarah P. Otto 0 2 0 Department of Zoology, University of British Columbia , Vancouver, British Columbia , Canada V6T 1Z4 1 Department of Entomology and Plant Pathology, Auburn University , Auburn, AL 36849 , USA 2 One contribution to a Special feature 'Evolution of specialization: insights from phylogenetic analysis' Evolutionary biologists have often assumed that ecological generalism comes at the expense of less intense exploitation of specific resources and that this trade-off will promote the evolution of ecologically specialized daughter species. Using a phylogenetic comparative approach with butterflies as a model system, we test hypotheses that incorporate changes in niche breadth and location into explanations of the taxonomic diversification of insect herbivores. Specifically, we compare the oscillation hypothesis, where speciation is driven by host-plant generalists giving rise to specialist daughter species, to the musical chairs hypothesis, where speciation is driven by host-plant switching, without changes in niche breadth. Contrary to the predictions of the oscillation hypothesis, we recover a negative relationship between hostplant breadth and diversification rate and find that changes in host breadth are seldom coupled to speciation events. By contrast, we present evidence for a positive relationship between rates of host switching and butterfly diversification, consonant with the musical chairs hypothesis. These results suggest that the costs of trophic generalism in plant-feeding insects may have been overvalued and that transitions from generalists to ecological specialists may not be an important driver of speciation in general. 1. Introduction About half of all eukaryotic species are plant-feeding insects [1]. The evolutionary processes that have driven the diversification of herbivorous insects are poorly understood, but host-plant interactions are thought to be a critical factor. The classic escape and radiate model of Ehrlich & Raven [2] intertwines the diversification of plants with that of the insects that eat them. This hypothesis assumes that plant diversity is limited by insect herbivore pressure and that herbivore diversity is limited by the nutrition and anti-herbivore defences of potential host plants. Under the escape and radiate model, plant or herbivore lineages that evolve ways to break free of these limitations diversify rapidly owing to their expanded ecological opportunities. Ehrlich and Raven did not specify a mechanism by which exposure to ecological opportunity would promote taxonomic diversification and, in point of fact, that mechanism remains uncertain [3]. Ecological opportunity is expected to result in ecological release, whereby selection becomes more diversifying and increased phenotypic variability is favoured. Yet theoretically, this release can lead either to many ecologically specialized species or to few ecologically generalized species, without rapid speciation [3,4]. Nevertheless, the escape and radiate model successfully predicts some patterns in biodiversity. In particular, the assumption that host-plant associations are instrumental in shaping the diversity of insect herbivores has been supported by a number of empirical studies. For example, Janz et al. [5] found a positive relationship between the species diversity of butterflies and the species diversity of their host-plant taxa, and Fordyce [6] reconstructed brief increases in butterfly diversification rates following major host shifts. One possible mechanism for turning ecological release into rapid species diversification centres on the idea that the jack of all trades is the master of none [7]. Diversifying selection regimes will tend to result in taxonomic diversification when there are non-trivial costs for broad niches, e.g. when increased trophic breadth strongly reduces the efficiency of resource use [8]. If we assume that there are fitness trade-offs associated with ecological generalism and that specialists do a better job in their niche than can a generalist, then generalism may be an ephemeral state [9,10]. In the context of plant-feeding insect diversification, this notion has been incorporated in the oscillation hypothesis [5,10]. Under this model, insect herbivore lineages undergo alternating phases of host expansion and contraction. Speciation is thought to be driven by the evolution of specialized populations from a more generalist ancestor, with episodic host-breadth expansions, replenishing the fuel consumed by speciation via specialization. Generalist species are not, however, the only source of new species, as specialists may switch specialties and expand into new adaptive zones without major changes in niche breadth [11]. We refer to this idea as the musical chairs hypothesis, which centres attention on host switching rather than on specialization. Taxonomic diversification of plant-feeding insects may thus be driven by the sheer diversity of niches associated with plants [12], allowing for multiple rounds of host switching. In this case, we expect lineages with more labile host associations to diversify more rapidly than those that switch hosts less often. Note the term musical chairs has been used before in the ecological literature to describe the impacts of interspecific competition on niche size and geographical distribution [13]. We do not intend to imply any connection between that and the hypothesis tested here. In this study, we use a comparative phylogenetic approach to test the impact of host breadth and lability on the diversification of butterflies (Papilionoidea). The oscillation and musical chairs hypotheses make different specific predictions about the effects of host breadth on diversification rates (table 1). The oscillation hypothesis predicts a positive relationship between host breadth and diversification rate, as it is the generalist ancestors that give rise to new specialist species. Because speciation is driven by host specialization, this hypothesis further predicts that speciation events should be associated with a trait shift from polyphagy to monophagy. That is, we would expect host specialization to involve cladogenetic shifts (associated with speciation events) rather than anagenetic shifts ( proportional to time). While not a strict prediction of the oscillation hypothesis, we also estimate the relative rates of transition to and from polyphagy, as this would determine how often lineages are likely to be in the generalist state promoting speciation. The musical chairs hypothesis predicts that diversification rates hinge strongly on aspects of butterfly biology that result in faster rates of host switching. Here, we do not attempt to identify specific traits that affect rates of host switching, but examples of such traits include trophic mode (e.g. external folivore, leaf miner (...truncated)