Discussion
Diaspidid species in tropical rainforest canopy habitats appear to use
as hosts only a small proportion of the plant taxa in their local
environment; simply put, diaspidids tend to be diet specialists. But
across the hundreds of trees that we surveyed, more specialized species
were no more abundant on their hosts than generalists, and occurred on a
smaller proportion of their potential host plants. Is specialization for
these diaspidids non-adaptive?
Such a conclusion would hinge on the assumption that what we saw within
the reach of canopy cranes is what we would have seen elsewhere. But if
abundance varies much over space, local differences in abundance could
be misleading. Some such heterogeneity is expected. The quality of
specific host-plant resources can vary due to spatial mosaics of natural
enemy pressure (Heard et al. 2006), as well as host-plant features such
as genotype, induced defensive state, and physical structure (Dixon
2005). Although we saw no abundant specialist species, each could have
been abundant somewhere else in the forest, where more suitable
resources occur. Nevertheless, extreme patchiness in the abundance of
specialists would entail a meta-population fitness cost, as local
catastrophes would be more likely to cause extinction (Nurmi & Parvinen
2008). In sum, potential spatial variation in abundance keeps us from
making definite conclusions about the adaptiveness of specificity in
diaspidids. But this potential is diminished by the cost of
meta-population patchiness, and the consistency of our observations
across species and communities.
We found that the use of many host taxa by diaspidids was
phylogenetically conservative. Although such conservatism of host use
has been found for several other groups of herbivorous insects, such as
butterflies (Janz et al. 2001) and beetles (Kelley and Farrell 1998), it
has a special significance for diaspidids, as they colonize new hosts
haphazardly via wind (Magsig-Castillo et al. 2010). Consequently, it may
more likely denote historical constraints on contemporary niches than
long-term persistence of niche optimization. In our previous work, we
found no evidence for performance trade-offs for diaspidids between
alternative hosts (Peterson et al. 2015); thus host-use constraints
would seem to persist in the face of what may be strong selection for
broad diets.
Our results also shed light on the complexity of host-use traits in
plant-feeding insects (Barrett and Heil 2012; Forister et al. 2012). We
found that specialization in armored scale insects occurs at all three
of the host-taxonomic levels that we considered (species, genus, and
family), suggesting that the genomic architecture of host-use traits is
both complex and hierarchical. Use of multiple hosts is often associated
with close phylogenetic relationships among those hosts (Gilbert and
Webb 2007; Krasnov et al. 2012), yet such results in flying insects may
reflect host-preference or ease of host recognition more than host
performance (Bernays 2001). Because diaspidids have little opportunity
to choose a host, phylogenetic conservatism at multiple taxonomic levels
implies that performance on a host likely depends on many traits of
various effect sizes. Although actual mechanisms are as yet unclear (but
see Hogenhout and Bos 2011; Ali and Agrawal 2012), the involvement of
many genetic loci in plant-insect interactions is consistent with both
ecological (Singer and Stireman 2005) and genetic (Remold 2012) theory
as well as recent genome-wide association studies (e.g., Egan et al.
2015; Gompter et al. 2015).
Our DNA-based species delimitation allow us some insight into whether
any species that have been characterized as extremely polyphagous
(Normark & Johnson 2011; Normark et al. 2014) are in fact clusters of
cryptic specialists. The answer is mixed. On the one hand, in Panama,
the single most polyphagous species in the sample, Selenaspidus
articulatus (Morgan) shows no hint of cryptic species diversity –
not surprisingly, as it is native to Africa and invasive in Panama
(Normark et al. 2019). On the other hand, several other reportedly
highly polyphagous species do appear to represent cryptic species
clusters. In Panama, only a single morphologically-delimited species
shows evidence of cryptic diversity: samples of Diaspis
boisduvalii (Signoret) were apportioned across five DNA-delimited
species. In contrast, at the Malaysian site, cryptic diversity appears
rampant, especially among the most polyphagous species:Chrysomphalus dictyospermi (Morgan), purported to use 80 host
families worldwide, was recovered as two cryptic species;Chrysomphalus pinnulifer (Maskell), with 40 host families
worldwide, was also recovered as two cryptic species; Morganella
longispina (Morgan), 22 host families worldwide, three cryptic species;Aonidiella inornata McKenzie, 24 host families worldwide, three
cryptic species. We also found cryptic diversity in less polyphagous
Southeast Asian species: Silvestraspis uberifera (Lindinger),
three cryptic species, and Aulacaspis calcarata (Takagi), eight
cryptic species, as well as in several undescribed species. Most
strikingly, one undescribed species provisionally designatedSishanaspis ud4977 appears to comprise a complex of 10 cryptic
species. The upshot is that in Malaysia traditional morphology-based
species delimitation seems to miss much of the true diversity. But our
inferences about the extent and consequence of diet specificity in
diaspidids appear robust to how species are delimitated.
One other insight afforded by the morphological species identifications,
which may help explain difference in diet breadth and host occupancy
observed between the two sites, is the incidence of invasive species. At
the Malaysian site we found no genera native to regions other than
Southeast Asia, whereas in Panama nearly half of morphologically
identifiable individuals (77/180 = 43%) belong to invasive species
(Normark et al. 2019). In addition to Selenaspidus articulatus(sampled on 18 host species), these include several genetically uniform
populations that we sampled on multiple host species, includingLepidosaphes rubrovittata (Cockerell) (6 hosts),Chrysomphalus dictyospermi (4 hosts), Aspidiotus excisusGreen (3 hosts), and Lepidosaphes punicae Laing (3 hosts). Thus
the narrower diets and higher host occupancy in Panama could have
something to do with the relatively recent arrival of much of the
diaspidid fauna.
In conclusion, evolutionary fitness is notoriously difficult to measure.
We can not draw straight lines connecting it to differences in local
abundance and patch occupancy. It could be that for diaspidids the
quality of host resources is extremely uneven across tropical canopies,
and that for each of the specialists we sampled there was an unsampled
population booming somewhere else in the forest. Or it could simply be
that host specialization is not adaptive for wind-dispersed plant
pathogens in diverse host-plant communities. If host-use specialization
is adaptive and high quality hosts are patchy and rare, then the
question becomes this: where in the forest are all the specialists? What
are the conditions that must be met for a specialist to make good on
their specialty?