Introduction

Insects are the most diverse group of Eukaryotes with a vast variety of species being phytophagous and functionally classified in polyphagous, oligophagous and monophagous when feeding on plants from multiple families, from a single family or form a single species respectively . Contemporary host plant feeding preferences are generally well defined but shifts in host plant preferences have been reported in a variety of insects such as lepidopterans, beetles and grasshoppers (. The shift towards novel hosts results in ecological niche expansion and subsequent adaptation to the new host can promote genetic divergence between populations, possibly with the evolution of host races and eventually of new species . Host races have been reported in variety of insects such as beetles and grasshoppers ( and a classical text-book example of the evolution of host races is Rhagoletis pomonella (Diptera, Tephritidae), where host-shifts from hawthorn to apples have led to the evolution of genetically divergent populations with different feeding preferences . Host plant shift or expansion may also favour geographic range expansion (and vice versa ) due to the possibility of occupying novel ecological niches and a wider geographic distribution ( These processes are of major significance in agronomy and conservation biology as they can promote the emergence of new invasive species and agricultural pests (. In fact, the host shift of R. pomonella is considered as the main cause of the expansion of this species in the Northwest Pacific (.
While changes in insect feeding preferences have been documented in phytophagous insects, the mechanisms behind these processes remain to be clarified. In this context, the insect gut microbiome plays a central role in adaptation to novel host plants as it is of crucial importance for the complex interactions with insects metabolic pathways which ultimately affect insect fitness . The gut microbiome of phytophagous insects can help to (1) break down the complex polysaccharides of the host plant cell wall, (2) supplement nitrogen, vitamins and sterols to the nutritionally poor diets , and (3) detoxify host plant allelochemicals and insecticides . For example, the symbiotic bacterium “Candidatus Erwinia dacicola” is essential for the metabolism of larvae of the olive fly Bactrocera oleae (Rossi, 1790) (Diptera, Tephritidae) as it allows them to feed on unripe olives rich in allelochemicals . The geographic range expansion of the kudzu bug (Megacopta cribaria , Hemiptera: Plataspidae) in the United States has been related to genomic mutations in its symbiontIshikawaella which allowed the insect to attack soybean as a novel host plant . Likewise, the invasive spread of some bark beetle species (Coleoptera: Scolytinae) has been associated with compositional changes in their microbial and fungal symbionts .
Tephritid fruit flies are a diverse group of flies with herbivorous larvae, with several species being notorious agricultural pests . Recent studies have started to investigate the importance of their gut microbiomes. However, as most of these studies target laboratory colonies with depauperate microbiomes, their results might not be fully representative for what happens in the field . For example, laboratory lines of the olive fly, Bactrocera oleae often lack “Candidatus Erwinia dacicola” despite that this symbiont is crucial for larval survival and development on the olive host . Conversely, Acetobacter , Morganella andPaenibacillus can be found in laboratory lines of B. oleae , while these bacteria are not a relevant component of the gut microbiome of wild populations . In this respect, De Cock et al. (2020) reported that gut microbiomes of wild tephritid agricultural pests are highly heterogeneous and stressed the importance of local effects in shaping their diversity.
In this study, we focus on wild parental (F0) and semi-wild offspring (F1) samples of the frugivorous fruit fly Zeugodacus cucurbitae (Coquillett, 1899) (Diptera, Tephritidae). This widespread agricultural pest is commonly found in South and East Asia, Africa, in the islands of the Indian ocean and in Hawaii . It recently expanded from East to West Africa and to the islands in the Indian Ocean including La Réunion . Larvae of this oligophagous species typically feed on Cucurbitaceae, but occasionally they also attack a variety of “unconventional” host plants from different families, including Solanaceae . This, together with observed geographic range expansion in recent decades , raises concerns about the invasion risk of this species which might actually be polyphagous rather than oligophagous.
The objective of this study is to explore how the gut microbiome composition of the cucurbit-feeder Z. cucurbitae changes when it feeds on a non-cucurbit host plant and how gut microbiome assemblages could facilitate the use of novel host plants in this phytophagous agricultural pest.