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.