Population genomics of invasive fruit flies

Global change and trade with agricultural products have resulted in worldwide movement of species and created novel pests. Various fruit flies are among the most rapidly expanding species, and a small proportion of them, mostly in the family Tephritidae, turned into severe threats to food production around the globe. The Mediterranean fruit fly Ceratitis capitata is the most damaging representative of tephritids and is one of the most invasive insect pests worldwide. Fruit flies are formidable models for evolutionary studies of bioinvasions because of their very wide distribution, complex pattern of host dependence, complex mating behaviour and the large body of work on life history, host specificity, demographics, and behavioural and reproductive biology that has been established in the course of biocontrol measures. In this study C. capitata will be used for a genomic analysis to assess key parameters about dispersal, selection and mate choice that are of great importance to understand what factors drive these rapidly expanding populations and how they might be contained.

Our research project has three main aims, based on a population genomics approach, to study (a) the historical path of range expansion, (b) the genetic effects of sterile insect release in biocontrol, and (c) the evolutionary impact of insecticides on the population biology. Each of these questions will greatly profit from genome-wide analysis of sequence variation using the RAD technique. Unlike conventional approaches that only sample selected, presumed neutral gene segments, genetic scans using RAD polymorphisms provide markers distributed fairly evenly across all parts of a genome. The method therefore has the advantages of whole genome sequencing, which remains prohibitive for many applications in terms of cost and data handling, but samples a proportion of the genomic variation sufficient for most purposes.

To our knowledge, this is the first population genomics approach to tephritid biology. This study therefore complements a vast literature on the ecological and evolutionary studies conducted in this group. The medfly, as the most prominent representative of this group, is a highly polyphagous and important agricultural pest species causing tremendous economic loss in the fruit production sector, and we therefore expect interest from biologists involved in applied and non-applied research. As already pointed out by Gasperi et al. (2002) "The analysis of the intrinsic variability of the medfly's genome and the genetic relationships among populations of this pest is a prerequisite for any control programme."

Here, we will first test the utility of RAD tags in phylogenetic reconstruction of the recent rapid range expansion of C. capitata that may be complicated by multiple eradications and re-invasions (e.g. in California); only a very large number of loci can be expected to overcome the inherent gene tree-species tree incongruence due to stochastic lineage sorting expected in single-gene studies. Our study therefore will contribute to testing the resolution of SNP variation, given a particular number of RAD tags obtained, and show what is the degree of incongruence among loci (as a measure of stochastic effects of lineage sorting). Information on the origin of populations in localities around the world is also of great practical relevance, as it identifies the source areas and routes of trade requiring quarantine measures.

Second, genome-wide scans provide novel ways of evaluating the effects of selection on population structure. Selective regimes result from the two major types of pest control, insecticides and SIT. The questions regarding the consequences of insecticide resistance are straightforward. Given a clearly defined phenotype, and a likely causative site in the Ace locus, what is the impact on the remainder of the genome? The mechanisms by which novel traits spread into existing populations by selective sweeps is of wide importance to understand the consequences of global change and the resulting range movements. Different scenarios are possible with regard to the portion of the genome that remains associated with the selected trait, and the potential loss of local adaptations elsewhere in the genome. Genomic population data therefore have great relevance for understanding the effectiveness of insecticides and the conservation of susceptible alleles locally. The C. capitata system will add an important case study to this debate.

Third, the use of SIT and of sex-lethal strains has been pioneered in C. capitata and remains of great theoretical and practical relevance. We are not aware of any existing studies that have investigated the population genomics in the wake of these treatments, neither from the perspective of the released incapacitated strains nor the impact on the target populations. Both aspects are important for the effectiveness of SIT, as they affect the performance and long-term success of these treatments. They also are relevant for the development of novel methods for introducing lethality into pest populations using a variety of genetic tools.

In short, a population genomics approach to the study of C. capitata comes at a perfect time as the RAD technique is now robustly applied to non-model organisms and the availability of the genome sequence for this species is imminent. The main impact of this study therefore will be by introducing a novel approach to a study organism of great importance, while the results are highly transferable to other systems, both in related tephritids, other Diptera (including malaria vectors in the genus Anopheles), and invasive species generally.