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?