BackgroundWe challenge the oft-repeated claim that the beetles (Coleoptera) are the most species-rich order of animals. Instead, we assert that another order of insects, the Hymenoptera, is more speciose, due in large part to the massively diverse but relatively poorly known parasitoid wasps. The idea that the beetles have more species than other orders is primarily based on their respective collection histories and the relative availability of taxonomic resources, which both disfavor parasitoid wasps. Though it is unreasonable to directly compare numbers of described species in each order, the ecology of parasitic wasps—specifically, their intimate interactions with their hosts—allows for estimation of relative richness.ResultsWe present a simple logical model that shows how the specialization of many parasitic wasps on their hosts suggests few scenarios in which there would be more beetle species than parasitic wasp species. We couple this model with an accounting of what we call the “genus-specific parasitoid–host ratio” from four well-studied genera of insect hosts, a metric by which to generate extremely conservative estimates of the average number of parasitic wasp species attacking a given beetle or other insect host species.ConclusionsSynthesis of our model with data from real host systems suggests that the Hymenoptera may have 2.5–3.2× more species than the Coleoptera. While there are more described species of beetles than all other animals, the Hymenoptera are almost certainly the larger order.Electronic supplementary materialThe online version of this article (10.1186/s12898-018-0176-x) contains supplementary material, which is available to authorized users.

The notion that shifts to new hosts can initiate insect speciation is more than 150 years old, yet widespread conflation with paradigms of sympatric speciation has led to confusion about how much support exists for this hypothesis. Here, we review 85 insect systems and evaluate the relationship between host shifting, reproductive isolation, and speciation. We sort insects into five categories: (1) systems in which a host shift has initiated speciation; (2) systems in which a host shift has made a contribution to speciation; (3) systems in which a host shift has caused the evolution of new reproductive isolating barriers; (4) systems with host-associated genetic differences; and (5) systems with no evidence of host-associated genetic differences. We find host-associated genetic structure in 65 systems, 43 of which show that host shifts have resulted in the evolution of new reproductive barriers. Twenty-six of the latter also support a role for host shifts in speciation, including eight studies that definitively support the hypothesis that a host shift has initiated speciation. While this review is agnostic as to the fraction of all insect speciation events to which host shifts have contributed, it clarifies that host shifts absolutely can and do initiate speciation.

4Background. We challenge the oft-repeated claim that the beetles (Coleoptera) are the most 1 5 species-rich order of animals. Instead, we assert that another order of insects, the Hymenoptera, 1 6 are more speciose, due in large part to the massively diverse but relatively poorly known 1 7 parasitoid wasps. The idea that the beetles have more species than other orders is primarily based 1 8 on their respective collection histories and the relative availability of taxonomic resources, which 1 9 3 1

1. Although divergence via host-plant shifting is a common theme in the speciation of some phytophagous insects, it is not clear whether host shifts are typically initiators of speciation or if they instead contribute to divergence events already in progress. While host shifts appear to be generally associated with speciation events for flies in the genus Strauzia, three sympatric varieties of the sunflower fly [Strauzia longipennis (Wiedemann)] co-occur on the same host plant in the Midwestern United States and may have evolved reproductive barriers without a host shift.2. The strength of two prezygotic reproductive barriers was compared among the three S. longipennis varieties: one barrier that is often associated with divergent ecological selection (allochronic isolation), and another that is more likely to be independent of ecological selection (pre-copulatory sexual isolation). The presence and relative strength of each barrier between fly varieties were evaluated using microsatellites, no choice mating experiments, studies of allochronic isolation, and field collection data.3. Evidence for both allochronic isolation and pre-copulatory sexual isolation was detected between the three varieties of S. longipennis. The measure of isolation calculated for each barrier between the three varieties was lower than measures calculated between different species of Strauzia found on different hosts, suggesting that subsequent host shifts may increase the degree of reproductive isolation. For Strauzia and other specialist insects, some reproductive isolation may evolve prior to, and indeed may facilitate, host shifts.

Congeneric parasites are unlikely to specialize on the same tissues of the same host species, likely because of strong multifarious selection against niche overlap. Exceptions where multiple congeneric species overlap on the same tissues may therefore reveal important insights into the ecological factors underlying the origins and maintenance of diversity. Larvae of sunflower maggot flies in genus Strauzia feed on the pith of plants in the family Asteraceae. Although Strauzia tend to be host specialists, some species overlap in their host use. To resolve the origins of host sharing among these specialist flies, we used reduced representation genomic sequencing to infer the first multi-locus phylogeny of genus Strauzia. Our results show that Helianthus tuberosus and Helianthus grosseserratus each host three different fly species, and that the flies co-occurring on a host are not one another's closest relatives. Though this pattern implies that host sharing is most likely the result of host shifts, these may not be host shifts in the conventional sense of an insect moving onto an entirely new plant. Many hosts of Strauzia belong to a young (1-2 MYA) clade of perennial sunflowers noted for their frequent introgression and hybrid speciation events. In at least one case, flies may have converged upon a host after their respective ancestral host plants hybridized to form a new sunflower species (H. tuberosus). Broadly, we suggest that rapid and recent adaptive introgression and speciation in this group of plants may have instigated the diversification of their phytophagous fly associates, including the convergence of >1 species onto the same shared host plants.