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

Zhang, Y. Miles; Sheikh, Sofia I.; Ward, Anna K G; Forbes, Andrew A.; Prior, Kirsten M.; Stone, Graham N.; Gates, Michael W.; Egan, Scott P.; Zhang, Linyi; Davis, Charles K.; Weinersmith, Kelly L.; Melika, George; Lucky, Andrea

doi:10.1111/mec.16582

Cited by 19 publications

(21 citation statements)

References 144 publications

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“…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.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2022

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Quantifying the frequency of shifts to new host plants within diverse clades of specialist herbivorous insects is critically important to understand whether and how host shifts contribute to the origin of species. Oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise a tribe of ∼1000 species of phytophagous insects that induce gall formation on various organs of trees in the family Fagacae-primarily the oaks (genus Quercus; ∼435 sp.). The association of oak gall wasps with oaks is ancient (∼50 my), and most oak species are galled by one or more gall wasp species. Despite the diversity of both gall wasp species and their plant associations, previous phylogenetic work has not identified the strong signal of host plant shifting among oak gall wasps that has been found in other phytophagous insect systems. However, most emphasis has been on the Western Palearctic and not the Nearctic where both oaks and oak gall wasps are considerably more species rich. We collected 86 species of Nearctic oak gall wasps from most of the major clades of Nearctic oaks and sequenced >1000 Ultraconserved Elements (UCEs) and flanking sequences to infer wasp phylogenies. We assessed the relationships of Nearctic gall wasps to one another and, by leveraging previously published UCE data, to the Palearctic fauna. We then used phylogenies to infer historical patterns of shifts among host tree species and tree organs. Our results indicate that oak gall wasps have moved between the Palearctic and Nearctic at least four times, that some Palearctic wasp clades have their proximate origin in the Nearctic, and that gall wasps have shifted within and between oak tree sections, subsections, and organs considerably more often than previous data have suggested. Given that host shifts have been demonstrated to drive reproductive isolation between host-associated populations in other phytophagous insects, our analyses of Nearctic gall wasps suggest that host shifts are key drivers of speciation in this clade, especially in hotspots of oak diversity. Although formal assessment of this hypothesis requires further study, two putatively oligophagous gall wasp species in our dataset

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Section: Discussionmentioning

confidence: 99%

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

et al. 2022

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“…This finding supports that niche specialization by generalist parasitoids with broad host ranges is common in oak gall wasp-parasitoid communities, with richness in parasitoid communities maintained by partitioning of generalist parasitoids among different gall phenotypes (24,42,51). However, with increased molecular studies of parasitoid wasp communities and their interactions, more putative specialists originally described as generalists are being revealed (27,28,53,93,94). Identifying parasitoids via morphological features and taxonomic keys is challenging, and rearing out parasitoids from hosts may lead to incomplete information about associations.…”

Section: Discussionmentioning

confidence: 99%

“…We also measured gall morphotype traits important in defense, such as gall size, internal traits (e.g., woody, fleshy or hollow), and external traits (e.g., nectar-producing, wooly, textured). We scored gall traits using our own observations and other resources (see S1 for details) (53,60,66).…”

Section: Host-parasitoid Interaction Traits and Phenologymentioning

confidence: 99%

“…Galls vary in traits, including size, shape, and texture, with several traits thought to be defensive adaptations to evade attack from natural enemies (43,(50)(51)(52). Host gall morphology and phenology influence the assemblages of enemies attacking host species (42,51,53). Oak gall wasp-enemy communities are tractable multi-trophic communities that are excellent systems for uncovering direct and indirect trophic interactions and how interactions are altered under anthropogenic change (18,23,38,(50)(51)(52)54,55).…”

Section: Introductionmentioning

confidence: 99%

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Host-enemy interactions provide limited biotic resistance for a range-expanding species via reduced apparent competition

Prior

Jones

Meadley‐Dunphy

et al. 2022

Preprint

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As species ranges shift in response to anthropogenic change, they lose coevolved or coadapted interactions and gain novel ones in recipient communities. Range-expanding species may lose or experience weak antagonistic interactions with competitors and enemies, and traits of interacting species will determine the strength of interactions. We leveraged a poleward range expansion of an oak gall wasp that co-occurs on its host plant with other gall wasp species and interacts with shared natural enemies (largely parasitoid wasps). We created quantitative host-parasitoid interaction networks by sampling galls on 400 trees. We compared network structure and function and traits of hosts and parasitoids in the native and expanded range. Interaction networks were less diverse in the expanded range, with low complementarity of parasitoid assemblages among hosts. While whole networks were more generalized in the expanded range, interactions with the range-expanding species were more specialized. This was not due to a loss of specialist enemies but weak apparent competition by shared generalist enemies. Phenological divergence of enemy assemblages attacking the novel and co-occurring hosts was greater in the expanded range that may contribute to weak apparent competition. Given the rate and extent of anthropogenic-driven range expansions, it is pressing to uncover how complex biotic interactions are reassembled.

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“…Meanwhile, other congeneric species can be very hard to distinguish, even for experienced taxonomists, and additionally, molecular data often reveal cryptic species (Cook et al, 2017; Haine et al, 2006; Molbo et al, 2003), as in many other insect taxa (e.g. moths – Hebert et al, 2004; bees – Mayr et al, 2021; and oak gall wasps – Zhang et al, 2022). Consequently, few community‐level studies have identified all wasps to species or even morphospecies level.…”

Section: Introductionmentioning

confidence: 99%

Insect community composition varies between temperate and tropical regions but functional structure remains conserved

DeGabriel

Sutton

Finch

et al. 2022

Insect Conserv Diversity

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1. Insect herbivores and their parasitoids make up a large proportion of biodiversity, but studies of their communities rarely involve geographic comparisons. If the community on a host plant varies geographically, insect diversity will be underestimated by ignoring this. In addition, community functional structure may vary geographically due to differential abundance of functional groups. 2. To address these issues, we compared the composition and structure of the fig wasp community associated with Ficus rubiginosa between temperate (Sydney) and tropical (Townsville) regions of eastern Australia. We sampled figs from four sites per region, twice a year for 2 years, resulting in about 14,000 wasps from 11 genera and 19 sub-generic taxa. Since two of these taxa each comprise two cryptic species, we refer to taxonomic diversity below, but this is largely at species level. 3. Taxonomic richness (14) was the same in both regions and nine taxa were shared across regions. However, 10 taxa were found in only one of the two regions, driving a significant difference in the taxonomic composition of the tropical and temperate communities, and increasing overall diversity in the system.4. The wasps belong to five functional groupspollinators, small and large gallers, and small and large parasitoids. In contrast to taxonomic composition and diversity, community functional structure did not differ significantly between regions. 5. Our results highlight that there can be broad latitudinal conservation of functional community structure across regions, despite considerable regional differences in taxonomic composition.

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

Cited by 19 publications

References 144 publications

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

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

Host-enemy interactions provide limited biotic resistance for a range-expanding species via reduced apparent competition

Insect community composition varies between temperate and tropical regions but functional structure remains conserved

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