Synergus

Ward, Anna K. G., Sheikh, Sofia I. & Forbes, Andrew A., 2020, Diversity, Host Ranges, and Potential Drivers of Speciation the Inquiline Enemies of Oak Gall Wasps (Hymenoptera: Cynipidae), Insect Systematics and Diversity 4 (6), No. 3, pp. 1-13 : 10

Implications for Synergus evolution

One leading explanation for why parasitoid wasps are so diverse is that adaptations to new insect hosts may lead to host-associated differentiation and speciation ( Stireman et al. 2005; Feder and Forbes 2010, Kaiser et al. 2015, König et al. 2015). When a parasitoid adopts a new host, trade-offs associated with adaptation to the new host can result in reproductive isolation from individuals attacking the ancestral host ( Hood et al. 2015). We know surprisingly little about whether the same ecological differences can drive lineage divergence in insect inquilines: one exception is the tumbling flower beetle Mordellistena convicta ( Coleoptera : Mordellidae ), which feeds on the galls of two lineages of Eurosta solidaginis gall flies ( Diptera : Tephritidae ) on goldenrods ( Solidaginis ; Compositae). Life history and molecular work has shown that both E. solidaginis and M. convicta have formed host-associated lineages on two different species of goldenrod, suggesting that speciation has ‘cascaded’ across trophic levels (gall former to inquiline) ( Abrahamson et al. 2003, Eubanks et al. 2003, Rhodes et al. 2012). This beetle system offers a compelling hint that ecological changes might lead to lineage divergence in inquilines, but missing is a broader study of ecological and host use patterns within an entire inquiline clade.

What do we learn about the role of host shifts in Synergus evolution? Though not a comprehensive phylogenetic history of these species, our mtCOI tree of Nearctic Synergus ( Fig. 2 ; Supp Figs 47 and 50 [online only]) nevertheless suggests many historical shifts between host tree sections ( Quercus to Lobatae), between gall wasp species, and between gall morphologies. This is not a definitive signature that host shifts drive speciation in Synergus , but the broad correlation between ecological changes and the evolution of reproductive isolation suggests this as a leading hypothesis. Transitions among host wasps, galls, and tree sections all represent changes that—to differing extents—require the evolution of novel behaviors, life histories, and strategies for circumventing host defenses. The accumulation of such divergent characters in the context of different habitats has been shown to directly ( Craig et al. 1993, Forbes et al. 2005, Fujiyama et al. 2013, Doellman et al. 2019, Hood et al. 2019) and indirectly ( Nosil and Hohenlohe 2012) lead to the evolution of reproductive isolation in many different insect systems.

An alternative to the above hypothesis is that ecological divergence among Synergus occurs after reproductive isolation evolves between lineages. For instance, perhaps Synergus speciate in the absence of divergent ecological selection (e.g., Nosil and Flaxman 2011), and then later shift into new hosts or habitats upon secondary contact because partitioning of environments facilitates coexistence of ecologically similar sympatric species ( Dufour et al. 2017). One advantage of our renewed exploration of the Nearctic Synergus is that it suggests taxa for further study that may allow the disentanglement of these competing hypotheses. For instance, clades where individuals with little or no mtCOI differentiation have been reared from galls of different morphologies (e.g., clades 3, 9, 27) could be interrogated further. If experimental tests revealed significant host-associated reproductive isolation and/or population genetic analyses suggested evidence of host-associated genetic differentiation, these might support a hypothesis that difference in host use is contributing to divergence. Similarly, as new samples of Synergus from across a wider geographic area are added to this data set, an increasing role for geographic isolation might emerge between sister species.

Figures

Fig. 2. Overview of all data used in inferring Synergus species hypotheses for this study.Left:simplified mtCOI phylogeny of Synergus included in this study (see Supp Fig. 47 [online only] for full tree). Bold branches indicate support ≥0.9. ‘Clade’ describes putative species assignments based on the sum of information to the right of this column. Gray bars in ABGD (conservative [‘C’] and liberal [‘L’] partitions) and bPTP columns indicate assignments of individuals into groups by these respective algorithms. ‘Morphological ID’ refers to each collection’s similarity (or lack of similarity) to previously described species. ‘Gall host’, ‘oak section’,‘plant tissue(s)’, and ‘Host gall morphology’ refer to ecological characters for Synergus in each clade, and example photos of galls are shown in Fig. 6.