Eating eggplants as a cucurbit feeder: Dietary shifts affect the gut microbiome of the melon flyZeugodacus cucurbitae(Diptera, Tephritidae)

Abstract

While contemporary changes in feeding preferences have been documented in phytophagous insects, the mechanisms behind these processes remain to be fully clarified. In this context, the insect gut microbiome plays a central role in adaptation to novel host plants. The cucurbit frugivorous fruit fly Zeugodacus cucurbitae (Diptera, Tephritidae) has occasionally been reported on "unconventional" host plants from different families, including Solanaceae. In this study, we focus on wild parental (F 0 ) adults and semiwild first filial (F 1 ) larvae of Z. cucurbitae from multiple sites in La Réunion and explore how the gut microbiome composition changes when this fly is feeding on a noncucurbit host (Solanum melongena). Our analyses show nonobvious gut microbiome responses following the F 0 -F host shift and the 1 importance of not just diet but also local effects, which heavily affected the diversity and composition of microbiomes. We identified the main bacterial genera responsible for differences between treatments. These data further stress the importance of a careful approach when drawing general conclusions based on laboratory populations or inadequately replicated field samples.

Maternal and host effects mediate the adaptive expansion and contraction of the microbiome during ontogeny in a holometabolous, polyphagous insect

“…Furthermore, flies may share their microbiomes in common oviposition sites and through adult food (Guo et al, 2017; Zaada et al, 2019), and pupation occurs in the microbe‐rich soil habitat, in contrast to microbe‐poor vermiculite in the laboratory (Barraza et al, 2020). Recent reports show that in leaf beetles (Coleoptera: Chrysomelidae) generalists harbour a more diversified microbiota than specialists (Brunetti et al, 2022), that diet shifts (fruit host change) can alter less abundant taxa more than abundant ones and that rare taxa that do not belong to the core community may drive gut bacterial community composition (Benjamino et al, 2018; Hendrycks et al, 2022). Moreover, rare taxa contribute disproportionally to community dynamics through various mechanisms over time and in a variety of environments (Jousset et al, 2017; Shade et al, 2014).…”

Anna Karenina as a promoter of microbial diversity in the cosmopolitan agricultural pest Zeugodacus cucurbitae (Diptera, Tephritidae)

“…As observed for other fruit fly species, the microbial community patterns of Z . cucurbitae reported in the literature are quantitatively and qualitatively heterogeneous [ 27 , 29 , 30 , 77 – 84 ]. Asimakis et al [ 85 ] reported how Enterobacteriaceae, Dysgomonadaceae and Orbaceae were dominant families in field populations of Z .…”

“…cucurbitae . Hendrycks et al [ 29 ], used a more rigorous statistical framework [ 86 ] on larvae collected from the Morogoro area, from crops including those targeted by this study (watermelon and cucumber); they identified Enterobacter , Klebsiella , and Citrobacter as core genera for Z . cucurbitae .…”

“…cucurbitae ). Their microbial patterns were characterised via DNA metabarcoding of the V3 and V4 regions of 16S rRNA as described in Hendrycks et al [ 29 ]. After quality checking of the raw data using Fastqc [ 57 ], the DADA2 pipeline [ 58 ] was used for read filtering, trimming, demultiplexing and recovering Amplicon Sequence Variants (ASVs).…”

“…However, in tephritid agricultural pests, a crop effect is not always detectable as the dominant driver of microbial diversity. In fact, other and less obvious processes [ 28 ] and the effects of high spatial heterogeneity [ 29 , 30 ] interact as drivers of microbial diversity and contribute to the variability of patterns observed. The recent work of Jose et al [ 28 ] elegantly demonstrates how crop-induced adaptation and lineage-dependent maternal effects are two interacting drivers of microbial diversity in a cosmopolitan polyphagous fruit fly.…”