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.