Genetic structure and symbiotic profile of worldwide natural populations of the Mediterranean fruit fly, Ceratitis capitata

Abstract

Background The Mediterranean fruit fly, Ceratitis capitata, is a cosmopolitan agricultural pest of worldwide economic importance and a model for the development of the Sterile Insect Technique (SIT) for fruit flies of the Tephritidae family (Diptera). SIT relies on the effective mating of laboratory-reared strains and natural populations, and therefore requires an efficient mass-rearing system that will allow for the production of high-quality males. Adaptation of wild flies to an artificial laboratory environment can be accompanied by negative effects on several life history traits through changes in their genetic diversity and symbiotic communities. Such changes may lead to reduced biological quality and mating competitiveness in respect to the wild populations. Profiling wild populations can help understand, and maybe reverse, deleterious effects accompanying laboratory domestication thus providing insects that can efficiently and effectively support SIT application. Results In the present study, we analyzed both the genetic structure and gut symbiotic communities of natural medfly populations of worldwide distribution, including Europe, Africa, Australia, and the Americas. The genetic structure of 408 individuals from 15 distinct populations was analyzed with a set of commonly used microsatellite markers. The symbiotic communities of a subset of 265 individuals from 11 populations were analyzed using the 16S rRNA gene-based amplicon sequencing of single individuals (adults). Genetic differentiation was detected among geographically distant populations while adults originated from neighboring areas were genetically closer. Alpha and beta diversity of bacterial communities pointed to an overall reduced symbiotic diversity and the influence of the geographic location on the bacterial profile. Conclusions Our analysis revealed differences both in the genetic profile and the structure of gut symbiotic communities of medfly natural populations. The genetic analysis expanded our knowledge to populations not analyzed before and our results were in accordance with the existing scenarios regarding this species expansion and colonization pathways. At the same time, the bacterial communities from different natural medfly populations have been characterized, thus broadening our knowledge on the microbiota of the species across its range. Genetic and symbiotic differences between natural and laboratory populations must be considered when designing AW-IPM approaches with a SIT component, since they may impact mating compatibility and mating competitiveness of the laboratory-reared males. In parallel, enrichment from wild populations and/or symbiotic supplementation could increase rearing productivity, biological quality, and mating competitiveness of SIT-important laboratory strains.

Looking at the big picture: worldwide population structure and range expansion of the cosmopolitan pest Ceratitis capitata (Diptera, Tephritidae)

“…Two of the private haplotypes (M005 and M008) for the region only differed by two and three bases respectively from the M007 haplotype and likely arose within the region (Ruiz-Arce et al 2020). Another study by Nikolouli (2020) corroborates the link between the European continent and Central America and shows clear clustering of four European populations with four Central American populations, based on eight microsatellite markers. Additionally, a study by Karsten et al (2015) showed that Guatemala was likely colonized from Greece.…”

“…We caution the reader to consider that while diversity can support colonization time estimates, it is best interpreted together with other information such as historical reports. This work, together with the contribution by Nikolouli (2020), who used eight microsatellite loci, the work by Karsten et al (2015) and the more recent study by Ruiz-Arce et al (2020) who have both used mitochondrial DNA sequencing methods, render the most current view on medfly genetic diversity, geographic genetic structure and invasion pathways. Although we consider the current dataset as an informative instrument for investigating medfly invasion history, we note that it will benefit from resampling of populations and new collections to stay relevant in the future.…”

“…One species in particular, the Mediterranean fruit fly or medfly (Ceratitis capitata) is considered one of the most notorious invaders. It originates from tropical Sub-Saharan Africa (De Meyer et al 2004), but during the past century it has spread to other tropical and more temperate regions worldwide (Arias et al 2018;Malacrida et al 2007;Nikolouli 2020). Medfly is now established in northern Africa, the Mediterranean, Latin America, Australia and the Hawaiian islands (Barr 2009;Bonizzoni et al 2004;Malacrida et al 2007) and is annually detected in California (Bonizzoni et al 2001;Carey 1991;Carey et al 2017).…”

New Insights on the Zeugodacus cucurbitae (Coquillett) Bacteriome

“…Bacterial strains isolated from stable microbial communities of wild individuals can be provided to mass-reared insects as supplements, in an attempt to replicate the natural microbiome and improve fitness and mating success [ 5 , 6 , 7 ]. Studies dealing with tephritid microbiomics use either samples from laboratory colonies [ 8 , 9 , 10 , 11 , 12 , 13 ] or wild populations [ 10 , 14 , 15 , 16 , 17 , 18 ], which are generally characterized by higher microbial diversity compared to laboratory strains [ 10 , 19 ]. Therefore, it is important to identify and exploit this large portion of diversity, but also to determine how it is affected by the geographical isolation of wild populations.…”

Characterisation of the symbionts in the Mediterranean fruitfly gut

“…These findings are consistent with previous analyses of medfly microbiomes made using culture-based methods (Behar et al 2005;Behar et al 2008a;Behar et al 2008b;Behar et al 2009a). The picture may be more complex, however, as one recent next-generation sequencing study did not isolate Klebsiella in medfly microbiomes from wild populations (Malacrinò et al 2018), and another identified possible geographic or host-genetic structure links with bacterial dominance (with samples from Greece being dominated by Klebsiella spp) (Nikolouli et al 2020).…”