Introduction
High species diversity has been attributed to the partitioning of available resources into narrow ecological niches (Hutchinson 1959). Yet niche width varies greatly between species. Herbivorous insects are classic subjects for the study of this variation. Although diet specialists prevail, diet breadths vary continuously, and some generalists are extremely so (Normark and Johnson 2011; Forister et al. 2015). How did this come to be?
For the most part, theorists have worked from the premise that diet specialization comes from genetic trade-offs between adaptations to alternative resources, specifically antagonistic pleiotropy between alleles at a few diet-determining loci (Futuyma and Moreno 1988; Ravigné et al. 2009). Although empirical evidence for such genetic trade-offs is scarce (Futuyma 2008; Forister et al. 2012), they might be difficult to detect, as they can be hidden by inter-individual fitness variation at linked loci (Joshi and Thompson 1995), or arise from epistatic interactions between alleles (Remold 2012; Rodriguez-Verdugo et al. 2014; Celorio-Mancera et al. 2016). In sum, the evidence is scarce for the adaptive trade-off hypothesis, but it is difficult to falsify outright.
Alternatively, niche specialization could be driven by non-adaptive processes (Futuyma et al. 1995; Gompert et al. 2015). In fact, theoretical spatial models have shown that adaptive trade-offs are not necessary to produce niche-breadth distributions resembling those observed in natural communities (Forister and Jenkins 2017). Evolving the ability to use a novel host almost certainly entails directional selection. But alleles promoting fitness on other potential hosts can be lost through genetic draft during strong directional selection on a novel host (Neher 2013), or genetic drift when insect and host distributions cease to overlap (Gompert et al. 2015). One way or another, if host-use traits are easy to lose but difficult to get back, neutral genetic processes could pull populations towards niche specialization (Hardy et al. 2016).
Host-use trade-offs in herbivorous insects have traditionally been investigated by comparing performance across multiple host plants of different insect genotypes within a population. But a phylogenetically-informed comparison of host-use across multiple herbivore species offers a complementary perspective that may be less obscured by short-term genetic contingencies (Funk et al. 1995; Futuyma 2010; Hardy and Otto 2014; Peterson et al. 2015, 2016). To wit, it could illuminate the overall relationship between diet-breadth and ecological performance. If host-use specificity is adaptive, we would expect that on any shared host specialists would tend to perform better than generalists. Likewise, at the meta-population level, if host-use specificity is adaptive, we might expect specialists to do a better job of colonizing specific host resources (Gryllenberg and Metz 2001). Conversely, if specificity is non-adaptive, we would expect generalists to colonize more of their potential hosts, and to perform just as well as specialists on shared hosts, or even perform better if there is a population-genetic cost for specificity, for example reduced population size and more erosive genetic drift.
We sought evidence of such performance differences in the relative abundances and patch occupancies of 171 putative armored scale insect species (Hemiptera: Diaspididae) across 138 tree species in tropical rainforest communities on two continents. Diaspidids are sessile and have a simple, pathogen-like life history in which new host trees are colonized by wind-dispersed first-instar nymphs that cannot survive for long away from a host (Hardy 2018). Potential for host-choice is therefore limited and occurrence of non-dispersive life stages on a plant is a relatively clear indication that it is a suitable host for development and reproduction (Hill and Holmes 2009). With random, time-limited dispersal, one might expect the greatest fitness for genotypes that perform best across most of the commonly encountered host-plants. In fact, for diaspidids, we have previously shown that when host associations are treated as a binary use-or-nonuse traits, the phylogenetic patterns of host use are incompatible with strong adaptive trade-offs (Peterson et al. 2015). Nevertheless, we have not previously been able to account for potentially important quantitative differences in performance across host plant groups.
Our approach was to (1) estimate allele genealogies among the sampled diaspidids for 3 loci, using DNA sequence data; (2) estimate species boundaries using these genealogies and also using morphology; (3) estimate the degree to which host use is phylogenetically conservative; (4) explicitly test for diet specialization in each species; and (5) use abundance-based and patch-occupancy-based indices of performance to test if specialists tend to do better than generalists on shared hosts.