Delimiting the cryptic diversity and host preferences of Sycophila parasitoid wasps associated with oak galls using phylogenomic data

Abstract

Cryptic species diversity is a major challenge for the species-rich community of parasitoids attacking oak gall wasps due to a high degree of sexual dimorphism, morphological plasticity, small size, and poorly known biology. As such, we know very little about the number of species present, nor the evolutionary forces responsible for generating this diversity. One hypothesis is that trait diversity in the gall wasps, including the morphology of the galls they induce, have evolved in response to selection imposed by the parasitoid community, with reciprocal selection driving diversification of the parasitoids. Using a rare continental scale data set of Sycophila parasitoid wasps reared from 44 species of cynipid galls from 18 species of oak across the US, we combined mitochondrial DNA barcodes, Ultraconserved Elements (UCEs), morphological, and natural history data to delimit putative species. We also generate the first large-scale assessment of ecological specialization and host association in this species-rich group with implications for evolutionary ecology and biocontrol. We find most Sycophila target multiple gall wasp species with similar gall morphologies and are generally associated with smaller galls. This result suggests that parasitoid wasps such as Sycophila have adaptations allowing them to exploit particular host trait combinations, while hosts with contrasting traits are resistant to attack. With our congruence-based method of species delimitation, our study has nearly doubled the number of Sycophila wasps among the lineages studied, which highlights the need for taxonomic revision of Sycophila, as many species cannot be identified morphologically or by using molecular delimitation methods.

The arthropod associates of 155 North American cynipid oak galls

“…Two clades from which no Sycophila were reared were a mixture of cluster galls on leaves and stems, early spring bud galls, and small monothalamous leaf galls. Sycophila appear to be reared more often from large galls (Figure 6e; Hall 2001, Zhang et al 2022) such that this apparent absence may reflect a general favoring of larger galls, but could also or instead be related to phenology or a bias in survivorship from smaller galls when using our rearing methods.…”

“…We keyed all emergent arthropods to superfamily, family, or, where possible, to genus (McAlpine et al 1981, Goulet and Huber 1993, Gibson et al 1997, Arnett et al 2000, 2002). Though species-level keys based on morphology exist for some Nearctic gall-associated genera, recent molecular analyses of three genera – Synergus Hartig, Ormyrus Westwood, and Sycophila Walker – have revealed much cryptic diversity in each genus (Ward et al 2020, Sheikh et al 2022, Zhang et al 2022), echoing similar work in the Palearctic (Ács et al 2002, Kaartinen et al 2010). Thus, to avoid incorrectly ascribing host associations of several putative specialist species to a single “lumped” species on the basis of morphology alone, we intentionally did not key many collections to species.…”

“…Due to the large size of these collections and our intention to use many in various future projects, we have not yet made a full set of voucher specimens available for study. However, vouchers for many of our gall wasps, and for wasps in the genera Synergus , Ormyrus, and Sycophila are already available (Ward et al 2020, Sheikh et al 2022, Ward et al 2022, Zhang et al 2022) and we intend to make vouchers of other genera available as more publications emerge from this dataset. Researchers interested in this material sooner than vouchers are made available may contact authors AAF, SPE, or KMP.…”

“…Two, several of the same insect natural enemy genera are known to be commonly reared from many different oak galls, and particular clades within each genus are known to specialize on oak galls (Gillette 1896, Balduf 1932, Grissell 1976, Hanson 1992, Lobato-Vila et al 2019). Three, studies employing DNA barcoding and sequencing of Ultraconserved Elements (UCE) paired with ecological data show more diversity, and more specialization on gall hosts, than had previously been suggested for some taxa (Ward et al 2020, Sheikh et al 2022, Zhang et al 2022). The data compiled and presented herein constitute a necessary step toward addressing coevolutionary (and other) hypotheses related to interactions between oak gall wasps and their insect associates.…”

Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both

“…Many parasitoids, inquilines, and hyperparasitoids have been reared from oak galls, with associates of some galls numbering more than 25 species (Joseph et al 2011, Bird et al 2013, Prior and Hellmann 2013, Forbes et al 2016, Weinersmith et al 2020). Recent work shows that many insect genera commonly associated with oak galls harbor species that specialize on one or a small subset of gall wasp hosts (Ward et al 2019, 2020, Sheikh et al 2022; Zhang et al 2022). If gall wasps shift hosts, and are followed by concomitant shifts by natural enemies, the ecological dimensions relevant to reproductive isolation in the gall wasp might “cascade” during a host-shift and promote reproductive isolation among insect natural enemies (Blair et al 2005, Stireman et al 2006, Abrahamson and Blair 2008, Forbes et al 2009, Hood et al 2015).…”